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Ravagni S, Montero-Mendieta S, Leonard JA, Webster MT, Christmas MJ, Bunikis I, Rodríguez-Teijeiro JD, Sanchez-Donoso I, Vilà C. Large Inversions Shape Diversification and Genome Evolution in Common Quails. Mol Ecol 2025; 34:e17740. [PMID: 40183764 DOI: 10.1111/mec.17740] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/01/2024] [Revised: 03/05/2025] [Accepted: 03/10/2025] [Indexed: 04/05/2025]
Abstract
Chromosomal inversions, by suppressing recombination, can profoundly shape genome evolution and drive adaptation. In the common quail (Coturnix coturnix), a highly mobile bird with a vast Palearctic breeding range, we previously identified a massive inversion on chromosome 1 associated with distinct phenotypes and restricted geographic distribution. Here, using a new de novo genome assembly, we characterise this inversion and uncover additional, ancient structural variation on chromosome 2 that segregates across the species' range: either two putatively linked inversions or a single, large inversion that appears as two due to scaffolding limitations. Together, the inversions encompass a remarkable 15.6% of the quail genome (153.6 Mbp), creating highly divergent haplotypes that diverged over a million years ago. While the chromosome 1 inversion is linked to phenotypic differences, including morphology and migratory behaviour, the chromosome 2 inversion(s) show no such association. Notably, all inversion regions exhibit reduced effective population size and a relaxation of purifying selection, evidenced by elevated nonsynonymous-to-synonymous substitution ratios (N/S). This suggests that inversions, particularly the geographically restricted one on chromosome 1, may act as engines of diversification, accelerating the accumulation of functional variation and potentially contributing to local adaptation, especially within isolated island populations. Our findings demonstrate how large-scale chromosomal rearrangements can compartmentalise a genome, fostering distinct evolutionary trajectories within a single, highly mobile species.
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Affiliation(s)
- Sara Ravagni
- Conservation and Evolutionary Genetics Group, Doñana Biological Station (EBD-CSIC), Seville, Spain
- Department of Biology and Biotechnologies "Charles Darwin", University of Rome La Sapienza, Rome, Italy
| | - Santiago Montero-Mendieta
- Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
| | - Jennifer A Leonard
- Conservation and Evolutionary Genetics Group, Doñana Biological Station (EBD-CSIC), Seville, Spain
| | - Matthew T Webster
- Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
| | - Matthew J Christmas
- Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
| | - Ignas Bunikis
- Uppsala Genome Center, Department of Immunology, Genetics and Pathology, Uppsala University, National Genomics Infrastructure Hosted by SciLifeLab, Uppsala, Sweden
| | | | - Ines Sanchez-Donoso
- Conservation and Evolutionary Genetics Group, Doñana Biological Station (EBD-CSIC), Seville, Spain
| | - Carles Vilà
- Conservation and Evolutionary Genetics Group, Doñana Biological Station (EBD-CSIC), Seville, Spain
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2
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Leishman EM, Vanderhout RJ, Wood BJ, Baes CF, Barbut S. Genome-wide association study to identify biological and metabolic pathways associated with carcass portion weights in turkeys: GWAS OF TURKEY CARCASS PORTION WEIGHTS. Poult Sci 2025; 104:105194. [PMID: 40300320 DOI: 10.1016/j.psj.2025.105194] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/16/2024] [Revised: 03/30/2025] [Accepted: 04/18/2025] [Indexed: 05/01/2025] Open
Abstract
The application of genetic and genomic improvement strategies in the poultry industry has been widely successful at improving meat yield and efficiency, however some challenges persist. As demand for larger and leaner birds increases, we have not fully assessed how selection for growth affects various carcass portions. The objective of this study was to conduct a genome wide association study (GWAS) and functional analysis on turkey carcass portion weights. Phenotypic data consisted of carcass portion weights (fillets, tenders, drums, thighs) obtained at processing (N = 646 - 1,478). Genotypic records were available from a proprietary 65 K single nucleotide polymorphism (SNP) chip. A linear mixed model was used to estimate SNP effects and a 30-SNP sliding window approach was used. Across all traits, 14 functional candidate genes (FCGs) were identified, and these were predominately associated with protein metabolism and immune function. Interestingly, carcass portions did not share FCGs, except for the thighs and drums, which shared one functional candidate gene (PDGFB). These results add to the understanding of the genetic architecture of carcass portion weights, and this could be applied in a turkey breeding program.
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Affiliation(s)
- Emily M Leishman
- Department of Animal Biosciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada; Department of Animal and Veterinary Sciences, Aarhus University, Tjele 8830, Denmark
| | - Ryley J Vanderhout
- Department of Animal Biosciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada; Hybrid Turkeys, Suite C, 650 Riverbend Drive, Kitchener, Ontario N2K 3S2, Canada
| | - Benjamin J Wood
- Department of Animal Biosciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada; School of Veterinary Science, University of Queensland, Gatton, Queensland 4343, Australia
| | - Christine F Baes
- Department of Animal Biosciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada; Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern 3001, Switzerland
| | - Shai Barbut
- Department of Food Science, University of Guelph, Guelph, Ontario N1G 2W1, Canada; Adaptation Physiology, Wageningen University, Wageningen 6700, the Netherlands.
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3
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Marín I. Vertebrate TNF Superfamily: Evolution and Functional Insights. BIOLOGY 2025; 14:54. [PMID: 39857285 PMCID: PMC11762692 DOI: 10.3390/biology14010054] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/21/2024] [Revised: 01/08/2025] [Accepted: 01/09/2025] [Indexed: 01/27/2025]
Abstract
This study characterizes the evolution of the tumor necrosis factor superfamily (TNFSF) across vertebrate lineages, both cyclostomes and gnathostomes, by combining sequence similarity and synteny data for the genes from 23 model species. The available evidence supports a simple model in which most of the diversity found in living species can be attributed to the expansion of four genes found in an ancestor of all vertebrates before the first of the genome duplications that occurred in the vertebrate lineages. It is inferred that the ancestor of all cyclostomes possessed only six TNFSF genes. A cyclostome-specific genome triplication had little effect on the total number of these genes. The ancestor of all gnathostomes, due to the effect of a second genome duplication plus additional single-gene duplications, already had 21 TNFSF genes. In several gnathostome lineages, particularly in some tetrapods, the TNF superfamily has significantly contracted due to numerous gene losses. This evolutionary model provides a framework for exploring functional data, showing that the descendants of different ancestral genes have acquired distinct roles, most prominently in the innate and adaptive immune systems, which led to a species-specific refinement of which TNFSF genes were conserved or lost. Several data hitherto difficult to interpret (the interactions of very different TNFSF ligands with the same receptors; the ability of the same ligands to bind alternative receptors, with or without death domains; and the cooperation of different ligands in specific functions) can be explained as consequences of the evolutionary history of the TNF superfamily.
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Affiliation(s)
- Ignacio Marín
- Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Científicas (IBV-CSIC), 46010 Valencia, Spain
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4
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Eaton DL, Williams DE, Coulombe RA. Species Differences in the Biotransformation of Aflatoxin B1: Primary Determinants of Relative Carcinogenic Potency in Different Animal Species. Toxins (Basel) 2025; 17:30. [PMID: 39852983 PMCID: PMC11768628 DOI: 10.3390/toxins17010030] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/10/2024] [Revised: 12/30/2024] [Accepted: 01/05/2025] [Indexed: 01/26/2025] Open
Abstract
It has been known since the early days of the discovery of aflatoxin B1 (AFB1) that there were large species differences in susceptibility to AFB1. It was also evident early on that AFB1 itself was not toxic but required bioactivation to a reactive form. Over the past 60 years there have been thousands of studies to delineate the role of ~10 specific biotransformation pathways of AFB1, both phase I (oxidation, reduction) and phase II (hydrolysis, conjugation, secondary oxidations, and reductions of phase I metabolites). This review provides a historical context and substantive analysis of each of these pathways as contributors to species differences in AFB1 hepatoxicity and carcinogenicity. Since the discovery of AFB1 as the toxic contaminant in groundnut meal that led to Turkey X diseases in 1960, there have been over 15,000 publications related to aflatoxins, of which nearly 8000 have addressed the significance of biotransformation (metabolism, in the older literature) of AFB1. While it is impossible to give justice to all of these studies, this review provides a historical perspective on the major discoveries related to species differences in the biotransformation of AFB1 and sets the stage for discussion of other papers in this Special Issue of the important role that AFB1 metabolites have played as biomarkers of exposure and effect in thousands of human studies on the toxic effects of aflatoxins. Dr. John Groopman has played a leading role in every step of the way-from initial laboratory studies on specific AFB1 metabolites to the application of molecular biomarkers in epidemiological studies associating dietary AFB1 exposure with liver cancer, and the design and conduct of chemoprevention clinical trials to reduce cancer risk from unavoidable aflatoxin exposures by alteration of specific AFB1 biotransformation pathways. This article is written in honor of Dr. Groopman's many contributions in this area.
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Affiliation(s)
- David L. Eaton
- Department of Environmental and Occupational Health Sciences, School of Public Health, University of Washington, Seattle, WA 98195, USA
| | - David E. Williams
- Environmental and Molecular Toxicology, College of Agricultural Sciences, Oregon State University, Corvalis, OR 97331, USA;
| | - Roger A. Coulombe
- Graduate Toxicology Program, Department of Veterinary Sciences, Utah State University, Logan, UT 84322, USA;
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Rabbani MAG, Vallejo-Trujillo A, Wu Z, Miedzinska K, Faruque S, Watson KA, Smith J. Whole genome sequencing of three native chicken varieties (Common Deshi, Hilly and Naked Neck) of Bangladesh. Sci Data 2024; 11:1432. [PMID: 39719437 DOI: 10.1038/s41597-024-04291-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/28/2024] [Accepted: 12/04/2024] [Indexed: 12/26/2024] Open
Abstract
Bangladeshi indigenous chicken varieties - Common Deshi, Hilly and Naked Neck are notable for their egg production, meat quality, extraordinary survivability and disease resistance. However, the potential to harness their unique genetic merits are being eroded by various factors, including crossbreeding. In-depth genomic studies have not been carried out on these breeds so far. To this end, blood samples and associated phenotypic metadata have been collected from local, unimproved birds sampled from 8 different locations across the country, and from Bangladesh Livestock Research Institute (BLRI)-improved chickens of the same mentioned breeds. Whole Genome Sequencing (WGS) of 96 selected samples, representing local and improved populations of each breed, has been carried out. Around 22 M high-quality SNPs have been identified, with 25% of these being novel variants previously undescribed in public databases. This data set will allow for genetic comparison between breeds, and between selected and unimproved birds, providing a resource for genomic selection in Bangladeshi breeding schemes to create more productive and resilient poultry stock.
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Affiliation(s)
- Md Ataul Goni Rabbani
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK.
- Poultry Production Research Division, Bangladesh Livestock Research Institute (BLRI), Savar, Dhaka, 1341, Bangladesh.
| | - Adriana Vallejo-Trujillo
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK
| | - Zhou Wu
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK
| | - Katarzyna Miedzinska
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK
| | - Shakila Faruque
- Poultry Production Research Division, Bangladesh Livestock Research Institute (BLRI), Savar, Dhaka, 1341, Bangladesh
| | - Kellie A Watson
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK
| | - Jacqueline Smith
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK
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6
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Husien HM, Saleh AA, Hassanine NNAM, Rashad AMA, Sharaby MA, Mohamed AZ, Abdelhalim H, Hafez EE, Essa MOA, Adam SY, Chen N, Wang M. The Evolution and Role of Molecular Tools in Measuring Diversity and Genomic Selection in Livestock Populations (Traditional and Up-to-Date Insights): A Comprehensive Exploration. Vet Sci 2024; 11:627. [PMID: 39728967 DOI: 10.3390/vetsci11120627] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/27/2024] [Revised: 12/03/2024] [Accepted: 12/04/2024] [Indexed: 12/28/2024] Open
Abstract
Distinctive molecular approaches and tools, particularly high-throughput SNP genotyping, have been applied to determine and discover SNPs, potential genes of interest, indicators of evolutionary selection, genetic abnormalities, molecular indicators, and loci associated with quantitative traits (QTLs) in various livestock species. These methods have also been used to obtain whole-genome sequencing (WGS) data, enabling the implementation of genomic selection. Genomic selection allows for selection decisions based on genomic-estimated breeding values (GEBV). The estimation of GEBV relies on the calculation of SNP effects using prediction equations derived from a subset of individuals in the reference population who possess both SNP genotypes and phenotypes for target traits. Compared to traditional methods, modern genomic selection methods offer advantages for sex-limited traits, low heritability traits, late-measured traits, and the potential to increase genetic gain by reducing generation intervals. The current availability of high-density genotyping and next-generation sequencing data allow for genome-wide scans for selection. This investigation provides an overview of the essential role of advanced molecular tools in studying genetic diversity and implementing genomic selection. It also highlights the significance of adaptive selection in light of new high-throughput genomic technologies and the establishment of selective comparisons between different genomes. Moreover, this investigation presents candidate genes and QTLs associated with various traits in different livestock species, such as body conformation, meat production and quality, carcass characteristics and composition, milk yield and composition, fertility, fiber production and characteristics, and disease resistance.
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Affiliation(s)
- Hosameldeen Mohamed Husien
- Laboratory of Metabolic Manipulation of Herbivorous Animal Nutrition, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China
- College of Veterinary Medicine, Albutana University, Rufaa 22217, Sudan
| | - Ahmed A Saleh
- College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China
- Animal and Fish Production Department, Faculty of Agriculture (Al-Shatby), Alexandria University, Alexandria 11865, Egypt
| | - Nada N A M Hassanine
- College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China
- Animal and Fish Production Department, Faculty of Agriculture (Al-Shatby), Alexandria University, Alexandria 11865, Egypt
| | - Amr M A Rashad
- Animal and Fish Production Department, Faculty of Agriculture (Al-Shatby), Alexandria University, Alexandria 11865, Egypt
| | - Mahmoud A Sharaby
- Animal and Fish Production Department, Faculty of Agriculture (Al-Shatby), Alexandria University, Alexandria 11865, Egypt
| | - Asmaa Z Mohamed
- Animal and Fish Production Department, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria 21531, Egypt
| | - Heba Abdelhalim
- Animal Production Research Institute, Agriculture Research Centre, Giza 12126, Egypt
| | - Elsayed E Hafez
- Arid Lands Cultivation Research Institute, City of Scientific Research and Technological Applications, New Borg El Arab, Alexandria 21934, Egypt
| | - Mohamed Osman Abdalrahem Essa
- College of Veterinary Medicine, Albutana University, Rufaa 22217, Sudan
- College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, China
| | - Saber Y Adam
- College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China
| | - Ning Chen
- State Key-Laboratory of Sheep Genetic Improvement and Healthy-Production, Xinjiang Academy of Agricultural Reclamation Sciences, Shihezi 832000, China
| | - Mengzhi Wang
- Laboratory of Metabolic Manipulation of Herbivorous Animal Nutrition, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China
- State Key-Laboratory of Sheep Genetic Improvement and Healthy-Production, Xinjiang Academy of Agricultural Reclamation Sciences, Shihezi 832000, China
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7
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Zhou Y, Mabrouk I, Ma J, Liu Q, Song Y, Xue G, Li X, Wang S, Liu C, Hu J, Sun Y. Chromosome-level genome sequencing and multi-omics of the Hungarian White Goose (Anser anser domesticus) reveals novel miRNA-mRNA regulation mechanism of waterfowl feather follicle development. Poult Sci 2024; 103:103933. [PMID: 38943801 PMCID: PMC11261457 DOI: 10.1016/j.psj.2024.103933] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/12/2024] [Revised: 05/07/2024] [Accepted: 05/29/2024] [Indexed: 07/01/2024] Open
Abstract
The Hungarian White Goose (Anser anser domesticus) is an excellent European goose breed, with high feather and meat production. Despite its importance in the poultry industry, no available genome assembly information has been published. This study aimed to present Chromosome-level and functional genome sequencing of the Hungarian White Goose. The results showed that the genome assembly has a total length of 1115.82 Mb, 39 pairs of chromosomes, 92.98% of the BUSCO index, and contig N50 and scaffold N50 were up to 2.32 Mb and 60.69 Mb, respectively. Annotation of the genome assembly revealed 19550 genes, 286 miRNAs, etc. We identified 235 expanded and 1,167 contracted gene families in this breed compared with the other 16 species. We performed a positive selection analysis between this breed and four species of Anatidae to uncover the genetic information underlying feather follicle development. Further, we detected the function of miR-199-x, miR-143-y, and miR-23-z on goose embryonic skin fibroblast. In summary, we have successfully generated a highly complete genome sequence of the Hungarian white goose, which will provide a great resource to improve our understanding of gene functions and enhance the studies on feather follicle development at the genomic level.
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Affiliation(s)
- Yuxuan Zhou
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Ichraf Mabrouk
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Jingyun Ma
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Qiuyuan Liu
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Yupu Song
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Guizhen Xue
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Xinyue Li
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Sihui Wang
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Chang Liu
- Changchun Municipal People's Government, Changchun Animal Husbandry Service, Changchun, 130062, China
| | - Jingtao Hu
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China
| | - Yongfeng Sun
- College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, China; Key Laboratory of Animal Production, Product Quality and Security, Jilin Agricultural University, Ministry of Education, Changchun, 130118, China..
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8
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Eleiwa A, Nadal J, Vilaprinyo E, Marin-Sanguino A, Sorribas A, Basallo O, Lucido A, Richart C, Pena RN, Ros-Freixedes R, Usie A, Alves R. Hybrid assembly and comparative genomics unveil insights into the evolution and biology of the red-legged partridge. Sci Rep 2024; 14:19531. [PMID: 39174643 PMCID: PMC11341709 DOI: 10.1038/s41598-024-70018-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/13/2024] [Accepted: 08/12/2024] [Indexed: 08/24/2024] Open
Abstract
The red-legged partridge Alectoris rufa plays a crucial role in the ecosystem of southwestern Europe, and understanding its genetics is vital for conservation and management. Here we sequence, assemble, and annotate a highly contiguous and nearly complete version of its genome. This assembly encompasses 96.9% of the avian genes flagged as essential in the BUSCO aves_odb10 dataset. Moreover, we pinpointed RNA and protein-coding genes, 95% of which had functional annotations. Notably, we observed significant chromosome rearrangements in comparison to quail (Coturnix japonica) and chicken (Gallus gallus). In addition, a comparative phylogenetic analysis of these genomes suggests that A. rufa and C. japonica diverged roughly 20 million years ago and that their common ancestor diverged from G. gallus 35 million years ago. Our assembly represents a significant advancement towards a complete reference genome for A. rufa, facilitating comparative avian genomics, and providing a valuable resource for future research and conservation efforts for the red-legged partridge.
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Affiliation(s)
| | | | - Ester Vilaprinyo
- Institut de Recerca Biomédica (IRBLleida), Lleida, Spain
- Universitat de Lleida (UdL), Lleida, Spain
| | - Alberto Marin-Sanguino
- Institut de Recerca Biomédica (IRBLleida), Lleida, Spain
- Universitat de Lleida (UdL), Lleida, Spain
| | - Albert Sorribas
- Institut de Recerca Biomédica (IRBLleida), Lleida, Spain
- Universitat de Lleida (UdL), Lleida, Spain
| | - Oriol Basallo
- Institut de Recerca Biomédica (IRBLleida), Lleida, Spain
- Universitat de Lleida (UdL), Lleida, Spain
| | - Abel Lucido
- Institut de Recerca Biomédica (IRBLleida), Lleida, Spain
- Universitat de Lleida (UdL), Lleida, Spain
| | | | - Ramona N Pena
- Universitat de Lleida (UdL), Lleida, Spain
- AGROTECNIO CERCA Center, Lleida, Spain
| | - Roger Ros-Freixedes
- Universitat de Lleida (UdL), Lleida, Spain
- AGROTECNIO CERCA Center, Lleida, Spain
| | - Anabel Usie
- Universitat de Lleida (UdL), Lleida, Spain
- Centro de Biotecnologia Agrícola e Agro-Alimentar do Alentejo (CEBAL)/Instituto Politécnico de Beja (IPBeja), Beja, Portugal
- MED-Instituto Mediterrâneo para a Agricultura, Ambiente e Desenvolvimento & CHANGE-Global Change and Sustainability Institute, Évora, Portugal
| | - Rui Alves
- Institut de Recerca Biomédica (IRBLleida), Lleida, Spain.
- Universitat de Lleida (UdL), Lleida, Spain.
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9
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Wanders K, Chen G, Feng S, Székely T, Urrutia AO. Role-reversed polyandry is associated with faster fast-Z in shorebirds. Proc Biol Sci 2024; 291:20240397. [PMID: 38864333 DOI: 10.1098/rspb.2024.0397] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/30/2023] [Accepted: 05/14/2024] [Indexed: 06/13/2024] Open
Abstract
In birds, males are homogametic and carry two copies of the Z chromosome ('ZZ'), while females are heterogametic and exhibit a 'ZW' genotype. The Z chromosome evolves at a faster rate than similarly sized autosomes, a phenomenon termed 'fast-Z evolution'. This is thought to be caused by two independent processes-greater Z chromosome genetic drift owing to a reduced effective population size, and stronger Z chromosome positive selection owing to the exposure of partially recessive alleles to selection. Here, we investigate the relative contributions of these processes by considering the effect of role-reversed polyandry on fast-Z in shorebirds, a paraphyletic group of wading birds that exhibit unusually diverse mating systems. We find stronger fast-Z effects under role-reversed polyandry, which is consistent with particularly strong selection on polyandrous females driving the fixation of recessive beneficial alleles. This result contrasts with previous research in birds, which has tended to implicate a primary role of genetic drift in driving fast-Z variation. We suggest that this discrepancy can be interpreted in two ways-stronger sexual selection acting on polyandrous females overwhelms an otherwise central role of genetic drift, and/or sexual antagonism is also contributing significantly to fast-Z and is exacerbated in sexually dimorphic species.
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Affiliation(s)
- Kees Wanders
- Department of Life Sciences, Milner Centre for Evolution, University of Bath , Bath, UK
- Department of Evolutionary Zoology and Human Biology, HUN-REN-DE Reproductive strategies Research Group, University of Debrecen , Debrecen, Hungary
- Natural History Museum of Denmark, University of Copenhagen , Copenhagen, Denmark
| | - Guangji Chen
- Center for Evolutionary & Organismal Biology, Liangzhu Laboratory, Department of General Surgery, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou, People's Republic of China
- BGI Research , Wuhan, People's Republic of China
- College of Life Sciences, University of Chinese Academy of Sciences , Beijing, People's Republic of China
| | - Shaohong Feng
- Center for Evolutionary & Organismal Biology, Liangzhu Laboratory, Department of General Surgery, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou, People's Republic of China
| | - Tamás Székely
- Department of Life Sciences, Milner Centre for Evolution, University of Bath , Bath, UK
- Department of Evolutionary Zoology and Human Biology, HUN-REN-DE Reproductive strategies Research Group, University of Debrecen , Debrecen, Hungary
- Debrecen Biodiversity Centre, University of Debrecen , Debrecen, Hungary
| | - Arraxi O Urrutia
- Department of Life Sciences, Milner Centre for Evolution, University of Bath , Bath, UK
- Instituto de Ecologia, UNAM , Mexico City, Mexico
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10
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Van Tassell CP, Rosen BD, Woodward-Greene MJ, Silverstein JT, Huson HJ, Sölkner J, Boettcher P, Rothschild MF, Mészáros G, Nakimbugwe HN, Gondwe TN, Muchadeyi FC, Nandolo W, Mulindwa HA, Banda LJ, Kaumbata W, Getachew T, Haile A, Soudre A, Ouédraogo D, Rischkowsky BA, Mwai AO, Dzomba EF, Nash O, Abegaz S, Masiga CW, Wurzinger M, Sayre BL, Stella A, Tosser-Klopp G, Sonstegard TS. The African Goat Improvement Network: a scientific group empowering smallholder farmers. Front Genet 2023; 14:1183240. [PMID: 37712066 PMCID: PMC10497955 DOI: 10.3389/fgene.2023.1183240] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/06/2023] [Accepted: 07/27/2023] [Indexed: 09/16/2023] Open
Abstract
The African Goat Improvement Network (AGIN) is a collaborative group of scientists focused on genetic improvement of goats in small holder communities across the African continent. The group emerged from a series of workshops focused on enhancing goat productivity and sustainability. Discussions began in 2011 at the inaugural workshop held in Nairobi, Kenya. The goals of this diverse group were to: improve indigenous goat production in Africa; characterize existing goat populations and to facilitate germplasm preservation where appropriate; and to genomic approaches to better understand adaptation. The long-term goal was to develop cost-effective strategies to apply genomics to improve productivity of small holder farmers without sacrificing adaptation. Genome-wide information on genetic variation enabled genetic diversity studies, facilitated improved germplasm preservation decisions, and provided information necessary to initiate large scale genetic improvement programs. These improvements were partially implemented through a series of community-based breeding programs that engaged and empowered local small farmers, especially women, to promote sustainability of the production system. As with many international collaborative efforts, the AGIN work serves as a platform for human capacity development. This paper chronicles the evolution of the collaborative approach leading to the current AGIN organization and describes how it builds capacity for sustained research and development long after the initial program funds are gone. It is unique in its effectiveness for simultaneous, multi-level capacity building for researchers, students, farmers and communities, and local and regional government officials. The positive impact of AGIN capacity building has been felt by participants from developing, as well as developed country partners.
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Affiliation(s)
- Curtis P. Van Tassell
- Animal Genomics and Improvement Laboratory, USDA Agricultural Research Service, Beltsville, MD, United States
| | - Benjamin D. Rosen
- Animal Genomics and Improvement Laboratory, USDA Agricultural Research Service, Beltsville, MD, United States
| | - M. Jennifer Woodward-Greene
- Animal Genomics and Improvement Laboratory, USDA Agricultural Research Service, Beltsville, MD, United States
- National Agricultural Library, USDA Agricultural Research Service, Beltsville, MD, United States
| | - Jeffrey T. Silverstein
- Office of National Programs, USDA Agricultural Research Service, Beltsville, MD, United States
| | - Heather J. Huson
- Department of Animal Science, Cornell University, Ithaca, NY, United States
| | - Johann Sölkner
- Division of Livestock Sciences, University of Natural Resources and Life Sciences, Vienna, Austria
| | - Paul Boettcher
- Animal Production and Health Division, Food and Agriculture Organization of the United Nations, Rome, Italy
| | - Max F. Rothschild
- Department of Animal Science, Iowa State University, Ames, IA, United States
| | - Gábor Mészáros
- Division of Livestock Sciences, University of Natural Resources and Life Sciences, Vienna, Austria
| | | | - Timothy N. Gondwe
- Department of Animal Science, Lilongwe University of Agriculture and Natural Resources, Lilongwe, Malawi
| | - Farai C. Muchadeyi
- Biotechnology Platform, Agricultural Research Council, Pretoria, South Africa
| | - Wilson Nandolo
- Department of Animal Science, Lilongwe University of Agriculture and Natural Resources, Lilongwe, Malawi
| | | | - Liveness J. Banda
- Department of Animal Science, Lilongwe University of Agriculture and Natural Resources, Lilongwe, Malawi
| | - Wilson Kaumbata
- Department of Animal Science, Lilongwe University of Agriculture and Natural Resources, Lilongwe, Malawi
| | - Tesfaye Getachew
- International Center for Agricultural Research in the Dry Areas, Addis Ababa, Ethiopia
| | - Aynalem Haile
- International Center for Agricultural Research in the Dry Areas, Addis Ababa, Ethiopia
| | - Albert Soudre
- Unité de Formation et de Recherches - Sciences et Technologies, Université Norbert ZONGO, Koudougou, Burkina Faso
| | | | | | | | - Edgar Farai Dzomba
- Discipline of Genetics, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa
| | - Oyekanmi Nash
- National Biotechnology Development Agency, Abuja, Nigeria
| | - Solomon Abegaz
- Ethiopian Institute of Agricultural Research, Addis Ababa, Ethiopia
| | | | - Maria Wurzinger
- Division of Livestock Sciences, University of Natural Resources and Life Sciences, Vienna, Austria
| | - Brian L. Sayre
- Department of Biology, Virginia State University, Petersburg, VA, United States
| | - Alessandra Stella
- Institute of Agricultural Biology and Biotechnology (IBBA), Milano, Italy
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11
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Rumore J, Walker M, Pagotto F, Forbes JD, Peterson CL, Tyler AD, Graham M, Van Domselaar G, Nadon C, Reimer A, Knox N. Use of a taxon-specific reference database for accurate metagenomics-based pathogen detection of Listeria monocytogenes in turkey deli meat and spinach. BMC Genomics 2023; 24:361. [PMID: 37370007 PMCID: PMC10303765 DOI: 10.1186/s12864-023-09338-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/02/2022] [Accepted: 04/26/2023] [Indexed: 06/29/2023] Open
Abstract
BACKGROUND The reliability of culture-independent pathogen detection in foods using metagenomics is contingent on the quality and composition of the reference database. The inclusion of microbial sequences from a diverse representation of taxonomies in universal reference databases is recommended to maximize classification precision for pathogen detection. However, these sizable databases have high memory requirements that may be out of reach for some users. In this study, we aimed to assess the performance of a foodborne pathogen (FBP)-specific reference database (taxon-specific) relative to a universal reference database (taxon-agnostic). We tested our FBP-specific reference database's performance for detecting Listeria monocytogenes in two complex food matrices-ready-to-eat (RTE) turkey deli meat and prepackaged spinach-using three popular read-based DNA-to-DNA metagenomic classifiers: Centrifuge, Kraken 2 and KrakenUniq. RESULTS In silico host sequence removal led to substantially fewer false positive (FP) classifications and higher classification precision in RTE turkey deli meat datasets using the FBP-specific reference database. No considerable improvement in classification precision was observed following host filtering for prepackaged spinach datasets and was likely a consequence of a higher microbe-to-host sequence ratio. All datasets classified with Centrifuge using the FBP-specific reference database had the lowest classification precision compared to Kraken 2 or KrakenUniq. When a confidence-scoring threshold was applied, a nearly equivalent precision to the universal reference database was achieved for Kraken 2 and KrakenUniq. Recall was high for both reference databases across all datasets and classifiers. Substantially fewer computational resources were required for metagenomics-based detection of L. monocytogenes using the FBP-specific reference database, especially when combined with Kraken 2. CONCLUSIONS A universal (taxon-agnostic) reference database is not essential for accurate and reliable metagenomics-based pathogen detection of L. monocytogenes in complex food matrices. Equivalent classification performance can be achieved using a taxon-specific reference database when the appropriate quality control measures, classification software, and analysis parameters are applied. This approach is less computationally demanding and more attainable for the broader scientific and food safety communities.
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Affiliation(s)
- Jillian Rumore
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada.
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada.
| | - Matthew Walker
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
| | - Franco Pagotto
- Food Directorate, Health Canada, Bureau of Microbial Hazards, Ottawa, ON, Canada
| | - Jessica D Forbes
- Eastern Ontario Regional Laboratory Association, Ottawa, ON, Canada
| | - Christy-Lynn Peterson
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
| | - Andrea D Tyler
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
| | - Morag Graham
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
| | - Gary Van Domselaar
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
| | - Celine Nadon
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
| | - Aleisha Reimer
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
| | - Natalie Knox
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada
- Public Health Agency of Canada, National Microbiology Laboratory, MB, Winnipeg, Canada
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12
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Gershman A, Hauck Q, Dick M, Jamison JM, Tassia M, Agirrezabala X, Muhammad S, Ali R, Workman RE, Valle M, Wong GW, Welch KC, Timp W. Genomic insights into metabolic flux in hummingbirds. Genome Res 2023; 33:703-714. [PMID: 37156619 PMCID: PMC10317124 DOI: 10.1101/gr.276779.122] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/21/2022] [Accepted: 04/26/2023] [Indexed: 05/10/2023]
Abstract
Hummingbirds are very well adapted to sustain efficient and rapid metabolic shifts. They oxidize ingested nectar to directly fuel flight when foraging but have to switch to oxidizing stored lipids derived from ingested sugars during the night or long-distance migratory flights. Understanding how this organism moderates energy turnover is hampered by a lack of information regarding how relevant enzymes differ in sequence, expression, and regulation. To explore these questions, we generated a chromosome-scale genome assembly of the ruby-throated hummingbird (A. colubris) using a combination of long- and short-read sequencing, scaffolding it using existing assemblies. We then used hybrid long- and short-read RNA sequencing of liver and muscle tissue in fasted and fed metabolic states for a comprehensive transcriptome assembly and annotation. Our genomic and transcriptomic data found positive selection of key metabolic genes in nectivorous avian species and deletion of critical genes (SLC2A4, GCK) involved in glucostasis in other vertebrates. We found expression of a fructose-specific version of SLC2A5 putatively in place of insulin-sensitive SLC2A5, with predicted protein models suggesting affinity for both fructose and glucose. Alternative isoforms may even act to sequester fructose to preclude limitations from transport in metabolism. Finally, we identified differentially expressed genes from fasted and fed hummingbirds, suggesting key pathways for the rapid metabolic switch hummingbirds undergo.
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Affiliation(s)
- Ariel Gershman
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21218, USA
- Department of Molecular Biology and Genetics, Johns Hopkins University, Baltimore, Maryland 21287, USA
| | - Quinn Hauck
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21218, USA
| | - Morag Dick
- Cell & Systems Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada
- Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, M1C 1A4, Canada
| | - Jerrica M Jamison
- Cell & Systems Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada
- Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, M1C 1A4, Canada
| | - Michael Tassia
- Department of Biology, Johns Hopkins University, Baltimore, Maryland 21218, USA
| | - Xabier Agirrezabala
- CIC bioGUNE, Basque Research and Technology Alliance (BRTA), 48160 Derio, Spain
| | - Saad Muhammad
- Cell & Systems Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada
- Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, M1C 1A4, Canada
| | - Raafay Ali
- Cell & Systems Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada
- Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, M1C 1A4, Canada
| | - Rachael E Workman
- Department of Molecular Biology and Genetics, Johns Hopkins University, Baltimore, Maryland 21287, USA
| | - Mikel Valle
- CIC bioGUNE, Basque Research and Technology Alliance (BRTA), 48160 Derio, Spain
| | - G William Wong
- Department of Physiology and Center for Metabolism and Obesity Research, School of Medicine, The Johns Hopkins University, Baltimore, Maryland 21205, USA
| | - Kenneth C Welch
- Cell & Systems Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada
- Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, M1C 1A4, Canada
| | - Winston Timp
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21218, USA;
- Department of Molecular Biology and Genetics, Johns Hopkins University, Baltimore, Maryland 21287, USA
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13
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Marlétaz F, de la Calle-Mustienes E, Acemel RD, Paliou C, Naranjo S, Martínez-García PM, Cases I, Sleight VA, Hirschberger C, Marcet-Houben M, Navon D, Andrescavage A, Skvortsova K, Duckett PE, González-Rajal Á, Bogdanovic O, Gibcus JH, Yang L, Gallardo-Fuentes L, Sospedra I, Lopez-Rios J, Darbellay F, Visel A, Dekker J, Shubin N, Gabaldón T, Nakamura T, Tena JJ, Lupiáñez DG, Rokhsar DS, Gómez-Skarmeta JL. The little skate genome and the evolutionary emergence of wing-like fins. Nature 2023; 616:495-503. [PMID: 37046085 PMCID: PMC10115646 DOI: 10.1038/s41586-023-05868-1] [Citation(s) in RCA: 21] [Impact Index Per Article: 10.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/23/2022] [Accepted: 02/21/2023] [Indexed: 04/14/2023]
Abstract
Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments1,2. However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins-including gene expression, chromatin occupancy and three-dimensional conformation-we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.
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Affiliation(s)
- Ferdinand Marlétaz
- Centre for Life's Origin and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK.
- Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Japan.
| | - Elisa de la Calle-Mustienes
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Rafael D Acemel
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
- Epigenetics and Sex Development Group, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany
| | - Christina Paliou
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Silvia Naranjo
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Pedro Manuel Martínez-García
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Ildefonso Cases
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Victoria A Sleight
- Department of Zoology, University of Cambridge, Cambridge, UK
- School of Biological Sciences, University of Aberdeen, Aberdeen, UK
| | | | - Marina Marcet-Houben
- Barcelona Supercomputing Centre (BCS-CNS), Barcelona, Spain
- Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain
| | - Dina Navon
- Department of Genetics, Rutgers the State University of New Jersey, Piscataway, NJ, USA
| | - Ali Andrescavage
- Department of Genetics, Rutgers the State University of New Jersey, Piscataway, NJ, USA
| | - Ksenia Skvortsova
- Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia
- Faculty of Medicine, St Vincent's Clinical School, University of New South Wales, Sydney, New South Wales, Australia
| | - Paul Edward Duckett
- Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia
| | - Álvaro González-Rajal
- Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia
- Faculty of Medicine, St Vincent's Clinical School, University of New South Wales, Sydney, New South Wales, Australia
| | - Ozren Bogdanovic
- Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia
| | - Johan H Gibcus
- Department of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA, USA
| | - Liyan Yang
- Department of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA, USA
| | - Lourdes Gallardo-Fuentes
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Ismael Sospedra
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Javier Lopez-Rios
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
| | - Fabrice Darbellay
- Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
- Department of Genetic Medicine and Development, Faculty of Medicine, University of Geneva, Geneva, Switzerland
| | - Axel Visel
- Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
- US Department of Energy Joint Genome Institute, Berkeley, CA, USA
- School of Natural Sciences, University of California, Merced, CA, USA
| | - Job Dekker
- Department of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA, USA
- Howard Hughes Medical Institute, Chevy Chase, MD, USA
| | - Neil Shubin
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA
| | - Toni Gabaldón
- Barcelona Supercomputing Centre (BCS-CNS), Barcelona, Spain
- Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain
- Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain
- CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, Madrid, Spain
| | - Tetsuya Nakamura
- Department of Genetics, Rutgers the State University of New Jersey, Piscataway, NJ, USA.
| | - Juan J Tena
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.
| | - Darío G Lupiáñez
- Epigenetics and Sex Development Group, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany.
| | - Daniel S Rokhsar
- Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Japan.
- Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA.
- Chan-Zuckerberg Biohub, San Francisco, CA, USA.
| | - José Luis Gómez-Skarmeta
- Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain
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14
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Shay JA, Haniford LSE, Cooper A, Carrillo CD, Blais BW, Lau CHF. Exploiting a targeted resistome sequencing approach in assessing antimicrobial resistance in retail foods. ENVIRONMENTAL MICROBIOME 2023; 18:25. [PMID: 36991496 PMCID: PMC10052294 DOI: 10.1186/s40793-023-00482-0] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/05/2022] [Accepted: 03/15/2023] [Indexed: 06/16/2023]
Abstract
BACKGROUND With the escalating risk of antimicrobial resistance (AMR), there are limited analytical options available that can comprehensively assess the burden of AMR carried by clinical/environmental samples. Food can be a potential source of AMR bacteria for humans, but its significance in driving the clinical spread of AMR remains unclear, largely due to the lack of holistic-yet-sensitive tools for surveillance and evaluation. Metagenomics is a culture-independent approach well suited for uncovering genetic determinants of defined microbial traits, such as AMR, present within unknown bacterial communities. Despite its popularity, the conventional approach of non-selectively sequencing a sample's metagenome (namely, shotgun-metagenomics) has several technical drawbacks that lead to uncertainty about its effectiveness for AMR assessment; for instance, the low discovery rate of resistance-associated genes due to their naturally small genomic footprint within the vast metagenome. Here, we describe the development of a targeted resistome sequencing method and demonstrate its application in the characterization of the AMR gene profile of bacteria associated with several retail foods. RESULT A targeted-metagenomic sequencing workflow using a customized bait-capture system targeting over 4,000 referenced AMR genes and 263 plasmid replicon sequences was validated against both mock and sample-derived bacterial community preparations. Compared to shotgun-metagenomics, the targeted method consistently provided for improved recovery of resistance gene targets with a much-improved target detection efficiency (> 300-fold). Targeted resistome analyses conducted on 36 retail-acquired food samples (fresh sprouts, n = 10; ground meat, n = 26) and their corresponding bacterial enrichment cultures (n = 36) reveals in-depth features regarding the identity and diversity of AMR genes, most of which were otherwise undetected by the whole-metagenome shotgun sequencing method. Furthermore, our findings suggest that foodborne Gammaproteobacteria could be the major reservoir of food-associated AMR genetic determinants, and that the resistome structure of the selected high-risk food commodities are, to a large extent, dictated by microbiome composition. CONCLUSIONS For metagenomic sequencing-based surveillance of AMR, the target-capture method presented herein represents a more sensitive and efficient approach to evaluate the resistome profile of complex food or environmental samples. This study also further implicates retail foods as carriers of diverse resistance-conferring genes indicating a potential impact on the dissemination of AMR.
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Affiliation(s)
- Julie A Shay
- Ottawa Laboratory (Carling), Canadian Food Inspection Agency, Ottawa, ON, Canada
| | - Laura S E Haniford
- Ottawa Laboratory (Carling), Canadian Food Inspection Agency, Ottawa, ON, Canada
| | - Ashley Cooper
- Ottawa Laboratory (Carling), Canadian Food Inspection Agency, Ottawa, ON, Canada
| | - Catherine D Carrillo
- Ottawa Laboratory (Carling), Canadian Food Inspection Agency, Ottawa, ON, Canada
| | - Burton W Blais
- Ottawa Laboratory (Carling), Canadian Food Inspection Agency, Ottawa, ON, Canada
| | - Calvin Ho-Fung Lau
- Ottawa Laboratory (Carling), Canadian Food Inspection Agency, Ottawa, ON, Canada.
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15
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Baloch AR, Feugang JM, Rodríguez-Osorio N. Editorial: Genomic and epigenomic applications in animal and veterinary sciences. Front Vet Sci 2023; 10:1167079. [PMID: 37020977 PMCID: PMC10069669 DOI: 10.3389/fvets.2023.1167079] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/15/2023] [Accepted: 03/01/2023] [Indexed: 03/22/2023] Open
Affiliation(s)
- Abdul Rasheed Baloch
- Panjwani Center for Molecular Medicine and Drug Research, International Center for Chemical and Biological Sciences, University of Karachi, Karachi, Pakistan
| | - Jean Magloire Feugang
- Department of Animal and Dairy Sciences, Mississippi State University, Starkville, MS, United States
| | - Nélida Rodríguez-Osorio
- Unidad de Genómica y Bioinformática, Departamento de Ciencias Biológicas, Universidad de la República, Salto, Uruguay
- *Correspondence: Nélida Rodríguez-Osorio
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16
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Mizushima S, Sasanami T, Ono T, Kuroiwa A. Current Approaches to and the Application of Intracytoplasmic Sperm Injection (ICSI) for Avian Genome Editing. Genes (Basel) 2023; 14:genes14030757. [PMID: 36981028 PMCID: PMC10048369 DOI: 10.3390/genes14030757] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/23/2023] [Revised: 03/10/2023] [Accepted: 03/17/2023] [Indexed: 03/30/2023] Open
Abstract
Poultry are one of the most valuable resources for human society. They are also recognized as a powerful experimental animal for basic research on embryogenesis. Demands for the supply of low-allergen eggs and bioreactors have increased with the development of programmable genome editing technology. The CRISPR/Cas9 system has recently been used to produce transgenic animals and various animals in the agricultural industry and has also been successfully adopted for the modification of chicken and quail genomes. In this review, we describe the successful establishment of genome-edited lines combined with germline chimera production systems mediated by primordial germ cells and by viral infection in poultry. The avian intracytoplasmic sperm injection (ICSI) system that we previously established and recent advances in ICSI for genome editing are also summarized.
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Affiliation(s)
- Shusei Mizushima
- Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo 060-0810, Japan
| | - Tomohiro Sasanami
- Faculty of Agriculture, Shizuoka University, 836 Ohya, Shizuoka 422-8529, Japan
| | - Tamao Ono
- Matsumoto Dental University, 1780 Gobara, Hiro-oka, Shiojiri 399-0781, Nagano, Japan
| | - Asato Kuroiwa
- Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo 060-0810, Japan
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17
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Integrative comparative analysis of avian chromosome evolution by in-silico mapping of the gene ontology of homologous synteny blocks and evolutionary breakpoint regions. Genetica 2023:10.1007/s10709-023-00185-x. [PMID: 36940055 DOI: 10.1007/s10709-023-00185-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/04/2023] [Accepted: 03/14/2023] [Indexed: 03/21/2023]
Abstract
Avian chromosomes undergo more intra- than interchromosomal rearrangements, which either induce or are associated with genome variations among birds. Evolving from a common ancestor with a karyotype not dissimilar from modern chicken, two evolutionary elements characterize evolutionary change: homologous synteny blocks (HSBs) constitute common conserved parts at the sequence level, while evolutionary breakpoint regions (EBRs) occur between HSBs, defining the points where rearrangement occurred. Understanding the link between the structural organization and functionality of HSBs and EBRs provides insight into the mechanistic basis of chromosomal change. Previously, we identified gene ontology (GO) terms associated with both; however, here we revisit our analyses in light of newly developed bioinformatic algorithms and the chicken genome assembly galGal6. We aligned genomes available for six birds and one lizard species, identifying 630 HSBs and 19 EBRs. We demonstrate that HSBs hold vast functionality expressed by GO terms that have been largely conserved through evolution. Particularly, we found that genes within microchromosomal HSBs had specific functionalities relevant to neurons, RNA, cellular transport and embryonic development, and other associations. Our findings suggest that microchromosomes may have conserved throughout evolution due to the specificity of GO terms within their HSBs. The detected EBRs included those found in the genome of the anole lizard, meaning they were shared by all saurian descendants, with others being unique to avian lineages. Our estimate of gene richness in HSBs supported the fact that microchromosomes contain twice as many genes as macrochromosomes.
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Smith J, Alfieri JM, Anthony N, Arensburger P, Athrey GN, Balacco J, Balic A, Bardou P, Barela P, Bigot Y, Blackmon H, Borodin PM, Carroll R, Casono MC, Charles M, Cheng H, Chiodi M, Cigan L, Coghill LM, Crooijmans R, Das N, Davey S, Davidian A, Degalez F, Dekkers JM, Derks M, Diack AB, Djikeng A, Drechsler Y, Dyomin A, Fedrigo O, Fiddaman SR, Formenti G, Frantz LA, Fulton JE, Gaginskaya E, Galkina S, Gallardo RA, Geibel J, Gheyas AA, Godinez CJP, Goodell A, Graves JA, Griffin DK, Haase B, Han JL, Hanotte O, Henderson LJ, Hou ZC, Howe K, Huynh L, Ilatsia E, Jarvis ED, Johnson SM, Kaufman J, Kelly T, Kemp S, Kern C, Keroack JH, Klopp C, Lagarrigue S, Lamont SJ, Lange M, Lanke A, Larkin DM, Larson G, Layos JKN, Lebrasseur O, Malinovskaya LP, Martin RJ, Martin Cerezo ML, Mason AS, McCarthy FM, McGrew MJ, Mountcastle J, Muhonja CK, Muir W, Muret K, Murphy TD, Ng'ang'a I, Nishibori M, O'Connor RE, Ogugo M, Okimoto R, Ouko O, Patel HR, Perini F, Pigozzi MI, Potter KC, Price PD, Reimer C, Rice ES, Rocos N, Rogers TF, Saelao P, Schauer J, Schnabel RD, Schneider VA, Simianer H, Smith A, et alSmith J, Alfieri JM, Anthony N, Arensburger P, Athrey GN, Balacco J, Balic A, Bardou P, Barela P, Bigot Y, Blackmon H, Borodin PM, Carroll R, Casono MC, Charles M, Cheng H, Chiodi M, Cigan L, Coghill LM, Crooijmans R, Das N, Davey S, Davidian A, Degalez F, Dekkers JM, Derks M, Diack AB, Djikeng A, Drechsler Y, Dyomin A, Fedrigo O, Fiddaman SR, Formenti G, Frantz LA, Fulton JE, Gaginskaya E, Galkina S, Gallardo RA, Geibel J, Gheyas AA, Godinez CJP, Goodell A, Graves JA, Griffin DK, Haase B, Han JL, Hanotte O, Henderson LJ, Hou ZC, Howe K, Huynh L, Ilatsia E, Jarvis ED, Johnson SM, Kaufman J, Kelly T, Kemp S, Kern C, Keroack JH, Klopp C, Lagarrigue S, Lamont SJ, Lange M, Lanke A, Larkin DM, Larson G, Layos JKN, Lebrasseur O, Malinovskaya LP, Martin RJ, Martin Cerezo ML, Mason AS, McCarthy FM, McGrew MJ, Mountcastle J, Muhonja CK, Muir W, Muret K, Murphy TD, Ng'ang'a I, Nishibori M, O'Connor RE, Ogugo M, Okimoto R, Ouko O, Patel HR, Perini F, Pigozzi MI, Potter KC, Price PD, Reimer C, Rice ES, Rocos N, Rogers TF, Saelao P, Schauer J, Schnabel RD, Schneider VA, Simianer H, Smith A, Stevens MP, Stiers K, Tiambo CK, Tixier-Boichard M, Torgasheva AA, Tracey A, Tregaskes CA, Vervelde L, Wang Y, Warren WC, Waters PD, Webb D, Weigend S, Wolc A, Wright AE, Wright D, Wu Z, Yamagata M, Yang C, Yin ZT, Young MC, Zhang G, Zhao B, Zhou H. Fourth Report on Chicken Genes and Chromosomes 2022. Cytogenet Genome Res 2023; 162:405-528. [PMID: 36716736 PMCID: PMC11835228 DOI: 10.1159/000529376] [Show More Authors] [Citation(s) in RCA: 16] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/16/2023] [Accepted: 01/22/2023] [Indexed: 02/01/2023] Open
Affiliation(s)
- Jacqueline Smith
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - James M. Alfieri
- Interdisciplinary Program in Ecology and Evolutionary Biology, Texas A&M University, College Station, Texas, USA
- Department of Biology, Texas A&M University, College Station, Texas, USA
- Department of Poultry Science, Texas A&M University, College Station, Texas, USA
| | | | - Peter Arensburger
- Biological Sciences Department, California State Polytechnic University, Pomona, California, USA
| | - Giridhar N. Athrey
- Interdisciplinary Program in Ecology and Evolutionary Biology, Texas A&M University, College Station, Texas, USA
- Department of Poultry Science, Texas A&M University, College Station, Texas, USA
| | | | - Adam Balic
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - Philippe Bardou
- Université de Toulouse, INRAE, ENVT, GenPhySE, Sigenae, Castanet Tolosan, France
| | | | - Yves Bigot
- PRC, UMR INRAE 0085, CNRS 7247, Centre INRAE Val de Loire, Nouzilly, France
| | - Heath Blackmon
- Interdisciplinary Program in Ecology and Evolutionary Biology, Texas A&M University, College Station, Texas, USA
- Department of Biology, Texas A&M University, College Station, Texas, USA
| | - Pavel M. Borodin
- Department of Molecular Genetics, Cell Biology and Bioinformatics, Institute of Cytology and Genetics of Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russian Federation
| | - Rachel Carroll
- Department of Animal Sciences, Data Science and Informatics Institute, University of Missouri, Columbia, Missouri, USA
| | | | - Mathieu Charles
- University Paris-Saclay, INRAE, AgroParisTech, GABI, Sigenae, Jouy-en-Josas, France
| | - Hans Cheng
- USDA, ARS, USNPRC, Avian Disease and Oncology Laboratory, East Lansing, Michigan, USA
| | | | | | - Lyndon M. Coghill
- Department of Veterinary Pathology, University of Missouri, Columbia, Missouri, USA
| | - Richard Crooijmans
- Animal Breeding and Genomics, Wageningen University and Research, Wageningen, The Netherlands
| | | | - Sean Davey
- University of Arizona, Tucson, Arizona, USA
| | - Asya Davidian
- Saint Petersburg State University, Saint Petersburg, Russian Federation
| | - Fabien Degalez
- Centre for Tropical Livestock Genetics and Health (CTLGH) − ILRI, Nairobi, Kenya
| | - Jack M. Dekkers
- Department of Animal Science, University of California, Davis, California, USA
- INRAE, MIAT UR875, Sigenae, Castanet Tolosan, France
| | - Martijn Derks
- Animal Breeding and Genomics, Wageningen University and Research, Wageningen, The Netherlands
| | - Abigail B. Diack
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - Appolinaire Djikeng
- Department of Molecular Microbiology and Immunology, University of Missouri, Columbia, Missouri, USA
| | | | - Alexander Dyomin
- Saint Petersburg State University, Saint Petersburg, Russian Federation
| | | | | | | | - Laurent A.F. Frantz
- Queen Mary University of London, Bethnal Green, London, UK
- Palaeogenomics Group, Department of Veterinary Sciences, LMU Munich, Munich, Germany
| | - Janet E. Fulton
- Hy-Line International, Research and Development, Dallas Center, Iowa, USA
| | - Elena Gaginskaya
- Saint Petersburg State University, Saint Petersburg, Russian Federation
| | - Svetlana Galkina
- Saint Petersburg State University, Saint Petersburg, Russian Federation
| | - Rodrigo A. Gallardo
- School of Veterinary Medicine, University of California, Davis, California, USA
- Department of Animal Science, University of California, Davis, California, USA
| | - Johannes Geibel
- Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Neustadt, Germany
- Center for Integrated Breeding Research, University of Göttingen, Göttingen, Germany
| | - Almas A. Gheyas
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - Cyrill John P. Godinez
- Department of Animal Science, College of Agriculture and Food Science, Visayas State University, Baybay City, Philippines
| | | | - Jennifer A.M. Graves
- Department of Environment and Genetics, La Trobe University, Melbourne, Victoria, Australia
- Institute for Applied Ecology, University of Canberra, Canberra, Australian Capital Territory, Australia
| | | | | | - Jian-Lin Han
- CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
- International Livestock Research Institute (ILRI), Addis Ababa, Ethiopia
| | - Olivier Hanotte
- International Livestock Research Institute (ILRI), Addis Ababa, Ethiopia
- Cells, Organisms and Molecular Genetics, School of Life Sciences, University of Nottingham, Nottingham, UK
- Centre for Tropical Livestock Genetics and Health, The Roslin Institute, Edinburgh, UK
| | - Lindsay J. Henderson
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - Zhuo-Cheng Hou
- National Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, MARA, College of Animal Science and Technology, China Agricultural University, Beijing, China
| | | | - Lan Huynh
- Institute for Immunology and Infection Research, University of Edinburgh, Edinburgh, UK
| | - Evans Ilatsia
- Dairy Research Institute, Kenya Agricultural and Livestock Organization, Naivasha, Kenya
| | | | | | - Jim Kaufman
- Institute for Immunology and Infection Research, University of Edinburgh, Edinburgh, UK
- Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
- Department of Pathology, University of Cambridge, Cambridge, UK
| | - Terra Kelly
- School of Veterinary Medicine, University of California, Davis, California, USA
- Department of Animal Science, University of California, Davis, California, USA
| | - Steve Kemp
- INRAE, INSTITUT AGRO, PEGASE UMR 1348, Saint-Gilles, France
| | - Colin Kern
- Feed the Future Innovation Lab for Genomics to Improve Poultry, University of California, Davis, California, USA
| | | | - Christophe Klopp
- Department of Animal Science, Iowa State University, Ames, Iowa, USA
| | - Sandrine Lagarrigue
- Centre for Tropical Livestock Genetics and Health (CTLGH) − ILRI, Nairobi, Kenya
| | - Susan J. Lamont
- Department of Animal Science, University of California, Davis, California, USA
- INRAE, MIAT UR875, Sigenae, Castanet Tolosan, France
| | - Margaret Lange
- Centre for Tropical Livestock Genetics and Health (CTLGH) − The Roslin Institute, Edinburgh, UK
| | - Anika Lanke
- College of Veterinary Medicine, Western University of Health Sciences, Pomona, California, USA
| | - Denis M. Larkin
- Department of Comparative Biomedical Sciences, Royal Veterinary College, University of London, London, UK
| | - Greger Larson
- The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, The University of Oxford, Oxford, UK
| | - John King N. Layos
- College of Agriculture and Forestry, Capiz State University, Mambusao, Philippines
| | - Ophélie Lebrasseur
- Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), CNRS UMR 5288, Université Toulouse III Paul Sabatier, Toulouse, France
- Instituto Nacional de Antropología y Pensamiento Latinoamericano, Ciudad Autónoma de Buenos Aires, Argentina
| | - Lyubov P. Malinovskaya
- Department of Cytology and Genetics, Novosibirsk State University, Novosibirsk, Russian Federation
| | - Rebecca J. Martin
- Saint Petersburg State University, Saint Petersburg, Russian Federation
| | | | | | | | - Michael J. McGrew
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
- Department of Molecular Microbiology and Immunology, University of Missouri, Columbia, Missouri, USA
| | | | - Christine Kamidi Muhonja
- Department of Veterinary Pathology, University of Missouri, Columbia, Missouri, USA
- Centre for Tropical Livestock Genetics and Health (CTLGH) − ILRI, Nairobi, Kenya
| | - William Muir
- Department of Animal Sciences, Purdue University, West Lafayette, Indiana, USA
| | - Kévin Muret
- Université Paris-Saclay, Commissariat à l'Energie Atomique et aux Energies Alternatives, Centre National de Recherche en Génomique Humaine, Evry, France
| | - Terence D. Murphy
- National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA
| | | | - Masahide Nishibori
- Laboratory of Animal Genetics, Graduate School of Integrated Sciences for Life, Hiroshima University, Higashi-Hiroshima, Japan
| | | | - Moses Ogugo
- Centre for Tropical Livestock Genetics and Health (CTLGH) − ILRI, Nairobi, Kenya
| | - Ron Okimoto
- Cobb-Vantress, Siloam Springs, Arkansas, USA
| | - Ochieng Ouko
- Department of Veterinary Pathology, University of Missouri, Columbia, Missouri, USA
| | - Hardip R. Patel
- The John Curtin School of Medical Research, Australian National University, Canberra, Australian Capital Territory, Australia
| | - Francesco Perini
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
- Department of Agricultural, Food and Environmental Sciences, University of Perugia, Perugia, Italy
| | - María Ines Pigozzi
- INBIOMED (CONICET-UBA), Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina
| | | | - Peter D. Price
- Ecology and Evolutionary Biology, School of Biosciences, University of Sheffield, Sheffield, UK
| | - Christian Reimer
- Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Neustadt, Germany
| | - Edward S. Rice
- Department of Animal Sciences, Bond Life Sciences Center, University of Missouri, Columbia, Missouri, USA
| | - Nicolas Rocos
- USDA, ARS, USNPRC, Avian Disease and Oncology Laboratory, East Lansing, Michigan, USA
| | - Thea F. Rogers
- Department of Molecular Evolution and Development, University of Vienna, Vienna, Austria
| | - Perot Saelao
- Department of Animal Science, University of California, Davis, California, USA
- Veterinary Pest Genetics Research Unit, USDA, Kerrville, Texas, USA
| | - Jens Schauer
- Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Neustadt, Germany
| | - Robert D. Schnabel
- Department of Animal Sciences, University of Missouri, Columbia, Missouri, USA
| | - Valerie A. Schneider
- National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA
| | - Henner Simianer
- Center for Integrated Breeding Research, University of Göttingen, Göttingen, Germany
| | - Adrian Smith
- Department of Zoology, University of Oxford, Oxford, UK
| | - Mark P. Stevens
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - Kyle Stiers
- Department of Veterinary Pathology, University of Missouri, Columbia, Missouri, USA
| | | | | | - Anna A. Torgasheva
- Department of Molecular Genetics, Cell Biology and Bioinformatics, Institute of Cytology and Genetics of Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russian Federation
| | - Alan Tracey
- University Paris-Saclay, INRAE, AgroParisTech, GABI, Sigenae, Jouy-en-Josas, France
| | - Clive A. Tregaskes
- Animal Breeding and Genomics, Wageningen University and Research, Wageningen, The Netherlands
- Saint Petersburg State University, Saint Petersburg, Russian Federation
| | - Lonneke Vervelde
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - Ying Wang
- Department of Animal Science, University of California, Davis, California, USA
| | - Wesley C. Warren
- Department of Animal Sciences, Bond Life Sciences Center, University of Missouri, Columbia, Missouri, USA
- Department of Animal Sciences, University of Missouri, Columbia, Missouri, USA
| | - Paul D. Waters
- School of Biotechnology and Biomolecular Science, Faculty of Science, UNSW Sydney, Sydney, New South Wales, Australia
| | - David Webb
- National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA
| | - Steffen Weigend
- Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Neustadt, Germany
- Center for Integrated Breeding Research, University of Göttingen, Göttingen, Germany
| | - Anna Wolc
- INRAE, MIAT UR875, Sigenae, Castanet Tolosan, France
- Hy-Line International, Research and Development, Dallas Center, Iowa, USA
| | - Alison E. Wright
- Ecology and Evolutionary Biology, School of Biosciences, University of Sheffield, Sheffield, UK
| | - Dominic Wright
- AVIAN Behavioural Genomics and Physiology, IFM Biology, Linköping University, Linköping, Sweden
| | - Zhou Wu
- The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh, UK
| | - Masahito Yamagata
- Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts, USA
| | | | - Zhong-Tao Yin
- Department of Animal Sciences, Data Science and Informatics Institute, University of Missouri, Columbia, Missouri, USA
| | | | - Guojie Zhang
- Center for Evolutionary and Organismal Biology, Zhejiang University School of Medicine, Hangzhou, China
| | - Bingru Zhao
- College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, China
| | - Huaijun Zhou
- Department of Animal Science, University of California, Davis, California, USA
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19
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Gugiu GB, Goto RM, Bhattacharya S, Delgado MK, Dalton J, Balendiran V, Miller MM. Mass Spectrometry Defines Lysophospholipids as Ligands for Chicken MHCY Class I Molecules. JOURNAL OF IMMUNOLOGY (BALTIMORE, MD. : 1950) 2023; 210:96-102. [PMID: 36427007 PMCID: PMC9772402 DOI: 10.4049/jimmunol.2200066] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/19/2022] [Accepted: 10/24/2022] [Indexed: 12/24/2022]
Abstract
Chicken (Gallus gallus) MHCY class I molecules are highly polymorphic yet substantially different from polymorphic MHC class I molecules that bind peptide Ags. The binding grooves in MHCY class I molecules are hydrophobic and too narrow to accommodate peptides. An earlier structural study suggested that ligands for MHCY class I might be lipids, but the contents of the groove were not clearly identified. In this study, lysophospholipids have been identified by mass spectrometry as bound in two MHCY class I isoforms that differ substantially in sequence. The two isoforms, YF1*7.1 and YF1*RJF34, differ by 35 aa in the α1 and α2 domains that form the MHC class I ligand binding groove. Lyso-phosphatidylethanolamine (lyso-PE) 18:1 was the dominant lipid identified in YF1*7.1 and YF1*RJF34 expressed as recombinant molecules and renatured with β2-microglobulin in the presence of a total lipid extract from Escherichia coli. Less frequently detected were lyso-PE 17:1, lyso-PE 16:1, and lysophosphatidylglycerols 17:1 and 16:0. These data provide evidence that lysophospholipids are candidate ligands for MHCY class I molecules. Finding that MHCY class I isoforms differing substantially in sequence bind the same array of lysophospholipids indicates that the amino acid polymorphism that distinguishes MHCY class I molecules is not key in defining ligand specificity. The polymorphic positions lie mostly away from the binding groove and might define specificity in interactions of MHCY class I molecules with receptors that are presently unidentified. MHCY class I molecules are distinctive in bound ligand and in display of polymorphic residues.
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Affiliation(s)
- Gabriel B. Gugiu
- Shared Resources, Mass Spectrometry Core, Beckman Research Institute, City of Hope, Duarte, CA
- Department of Molecular Immunology, Beckman Research Institute, City of Hope, Duarte, CA
| | - Ronald M. Goto
- Department of Molecular and Cellular Biology, Beckman Research Institute, City of Hope, Duarte, CA
| | - Supriyo Bhattacharya
- Shared Resources, Integrative Genomics Core, Beckman Research Institute, City of Hope, Duarte, CA
| | - Melissa K. Delgado
- Department of Molecular and Cellular Biology, Beckman Research Institute, City of Hope, Duarte, CA
- California State University, Long Beach, CA; and
| | - Jennifer Dalton
- Eugene and Ruth Roberts Summer Student Academy of City of Hope, Duarte, CA
| | | | - Marcia M. Miller
- Department of Molecular and Cellular Biology, Beckman Research Institute, City of Hope, Duarte, CA
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Barros CP, Derks MFL, Mohr J, Wood BJ, Crooijmans RPMA, Megens HJ, Bink MCAM, Groenen MAM. A new haplotype-resolved turkey genome to enable turkey genetics and genomics research. Gigascience 2022; 12:giad051. [PMID: 37489751 PMCID: PMC10360393 DOI: 10.1093/gigascience/giad051] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/21/2022] [Revised: 12/12/2022] [Accepted: 06/27/2023] [Indexed: 07/26/2023] Open
Abstract
BACKGROUND The domesticated turkey (Meleagris gallopavo) is a species of significant agricultural importance and is the second largest contributor, behind broiler chickens, to world poultry meat production. The previous genome is of draft quality and partly based on the chicken (Gallus gallus) genome. A high-quality reference genome of M. gallopavo is essential for turkey genomics and genetics research and the breeding industry. RESULTS By adopting the trio-binning approach, we were able to assemble a high-quality chromosome-level F1 assembly and 2 parental haplotype assemblies, leveraging long-read technologies and genome-wide chromatin interaction data (Hi-C). From a total of 40 chromosomes (2n = 80), we captured 35 chromosomes in a single scaffold, showing much improved genome completeness and continuity compared to the old assembly build. The 3 assemblies are of higher quality than the previous draft quality assembly and comparable to the chicken assemblies (GRCg7) shown by the largest contig N50 (26.6 Mb) and comparable BUSCO gene set completeness scores (96-97%). Comparative analyses confirm a previously identified large inversion of around 19 Mbp on the Z chromosome not found in other Galliformes. Structural variation between the parent haplotypes was identified, which poses potential new target genes for breeding. CONCLUSIONS We contribute a new high-quality turkey genome at the chromosome level, benefiting turkey genetics and other avian genomics research as well as the turkey breeding industry.
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Affiliation(s)
- Carolina P Barros
- Wageningen University and Research, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
| | - Martijn F L Derks
- Wageningen University and Research, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
| | - Jeff Mohr
- Hybrid Turkeys, 650 Riverbend Drive Suite C, Kitchener, ON N2K 3S2, Canada
| | - Benjamin J Wood
- Hybrid Turkeys, 650 Riverbend Drive Suite C, Kitchener, ON N2K 3S2, Canada
- School of Veterinary Science, University of Queensland, Gatton, QLD 4343, Australia
| | | | - Hendrik-Jan Megens
- Wageningen University and Research, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
| | - Marco C A M Bink
- Hendrix Genetics Research, Technology & Services, Boxmeer, AC 5830, The Netherlands
| | - Martien A M Groenen
- Wageningen University and Research, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
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21
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Ediriweera TK, Manjula P, Cho E, Kim M, Lee JH. Application of next-generation sequencing for the high-resolution typing of MHC-B in Korean native chicken. Front Genet 2022; 13:886376. [DOI: 10.3389/fgene.2022.886376] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/28/2022] [Accepted: 10/07/2022] [Indexed: 11/13/2022] Open
Abstract
The major histocompatibility complex-B (MHC-B) region of chicken is crucially important in their immunogenesis and highly diverse among different breeds, lines, and even populations. Because it determines the resistance/susceptibility to numerous infectious diseases, it is important to analyze this genomic region, particularly classical class I and II genes, to determine the variation and diversity that ultimately affect antigen presentation. This study investigated five lines of indigenous Korean native chicken (KNC) and the Ogye breed using next-generation sequencing (NGS) data with Geneious Prime-based assembly and variant calling with the Genome Analysis Toolkit (GATK) best practices pipeline. The consensus sequences of MHC-B (BG1-BF2) were obtained for each chicken line/breed and their variants were analyzed. All of the Korean native chicken lines possessed an excessive number of variants, including an ample amount of high-impact variants that provided useful information regarding modified major histocompatibility complex molecules. The study confirmed that next-generation sequencing techniques can effectively be used to detect MHC variabilities and the KNC lines are highly diverse for the MHC-B region, suggesting a substantial divergence from red junglefowl.
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22
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Zhang X, Hu Y, Smith DR. HSDatabase-a database of highly similar duplicate genes from plants, animals, and algae. Database (Oxford) 2022; 2022:baac086. [PMID: 36208223 PMCID: PMC9547538 DOI: 10.1093/database/baac086] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/05/2022] [Revised: 08/16/2022] [Accepted: 09/20/2022] [Indexed: 11/30/2022]
Abstract
Gene duplication is an important evolutionary mechanism capable of providing new genetic material, which in some instances can help organisms adapt to various environmental conditions. Recent studies, for example, have indicated that highly similar duplicate genes (HSDs) are aiding adaptation to extreme conditions via gene dosage. However, for most eukaryotic genomes HSDs remain uncharacterized, partly because they can be hard to identify and categorize efficiently and effectively. Here, we collected and curated HSDs in nuclear genomes from various model animals, land plants and algae and indexed them in an online, open-access sequence repository called HSDatabase. Currently, this database contains 117 864 curated HSDs from 40 distinct genomes; it includes statistics on the total number of HSDs per genome as well as individual HSD copy numbers/lengths and provides sequence alignments of the duplicate gene copies. HSDatabase also allows users to download sequences of gene copies, access genome browsers, and link out to other databases, such as Pfam and Kyoto Encyclopedia of Genes and Genomes. What is more, a built-in Basic Local Alignment Search Tool option is available to conveniently explore potential homologous sequences of interest within and across species. HSDatabase has a user-friendly interface and provides easy access to the source data. It can be used on its own for comparative analyses of gene duplicates or in conjunction with HSDFinder, a newly developed bioinformatics tool for identifying, annotating, categorizing and visualizing HSDs. Database URL: http://hsdfinder.com/database/.
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Affiliation(s)
- Xi Zhang
- Institute for Comparative Genomics, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
- Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada
| | - Yining Hu
- Department of Computer Science, University of Western Ontario, London, Ontario N6A 3K7, Canada
| | - David Roy Smith
- Department of Biology, University of Western Ontario, London, Ontario N6A 3K7, Canada
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23
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Liu S, Chen H, Ouyang J, Huang M, Zhang H, Zheng S, Xi S, Tang H, Gao Y, Xiong Y, Cheng D, Chen K, Liu B, Li W, Ren J, Yan X, Mao H. A high-quality assembly reveals genomic characteristics, phylogenetic status, and causal genes for leucism plumage of Indian peafowl. Gigascience 2022; 11:giac018. [PMID: 35383847 PMCID: PMC8985102 DOI: 10.1093/gigascience/giac018] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/29/2021] [Revised: 11/15/2021] [Accepted: 02/09/2022] [Indexed: 12/28/2022] Open
Abstract
BACKGROUND The dazzling phenotypic characteristics of male Indian peafowl (Pavo cristatus) are attractive both to the female of the species and to humans. However, little is known about the evolution of the phenotype and phylogeny of these birds at the whole-genome level. So far, there are no reports regarding the genetic mechanism of the formation of leucism plumage in this variant of Indian peafowl. RESULTS A draft genome of Indian peafowl was assembled, with a genome size of 1.05 Gb (the sequencing depth is 362×), and contig and scaffold N50 were up to 6.2 and 11.4 Mb, respectively. Compared with other birds, Indian peafowl showed changes in terms of metabolism, immunity, and skeletal and feather development, which provided a novel insight into the phenotypic evolution of peafowl, such as the large body size and feather morphologies. Moreover, we determined that the phylogeny of Indian peafowl was more closely linked to turkey than chicken. Specifically, we first identified that PMEL was a potential causal gene leading to the formation of the leucism plumage variant in Indian peafowl. CONCLUSIONS This study provides an Indian peafowl genome of high quality, as well as a novel understanding of phenotypic evolution and phylogeny of Indian peafowl. These results provide a valuable reference for the study of avian genome evolution. Furthermore, the discovery of the genetic mechanism for the development of leucism plumage is both a breakthrough in the exploration of peafowl plumage and also offers clues and directions for further investigations of the avian plumage coloration and artificial breeding in peafowl.
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Affiliation(s)
- Shaojuan Liu
- College of Animal Science, South China Agricultural University, Guangzhou 510642, China
| | - Hao Chen
- College of Life Science, Jiangxi Science & Technology Normal University, Nanchang 330013, China
| | - Jing Ouyang
- College of Life Science, Jiangxi Science & Technology Normal University, Nanchang 330013, China
| | - Min Huang
- College of Animal Science, South China Agricultural University, Guangzhou 510642, China
| | - Hui Zhang
- College of Animal Science, South China Agricultural University, Guangzhou 510642, China
| | - Sumei Zheng
- College of Animal Science, South China Agricultural University, Guangzhou 510642, China
| | - Suwang Xi
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China
| | - Hongbo Tang
- College of Life Science, Jiangxi Science & Technology Normal University, Nanchang 330013, China
| | - Yuren Gao
- College of Life Science, Jiangxi Science & Technology Normal University, Nanchang 330013, China
| | - Yanpeng Xiong
- College of Life Science, Jiangxi Science & Technology Normal University, Nanchang 330013, China
| | - Di Cheng
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China
| | - Kaifeng Chen
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China
| | - Bingbing Liu
- College of Animal Science, South China Agricultural University, Guangzhou 510642, China
| | - Wanbo Li
- Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Jimei University, Xiamen 361021, China
| | - Jun Ren
- College of Animal Science, South China Agricultural University, Guangzhou 510642, China
| | - Xueming Yan
- College of Life Science, Jiangxi Science & Technology Normal University, Nanchang 330013, China
| | - Huirong Mao
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China
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24
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Abdalla EAE, Makanjuola BO, Wood BJ, Baes CF. Genome-wide association study reveals candidate genes relevant to body weight in female turkeys (Meleagris gallopavo). PLoS One 2022; 17:e0264838. [PMID: 35271651 PMCID: PMC8912253 DOI: 10.1371/journal.pone.0264838] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/17/2021] [Accepted: 02/17/2022] [Indexed: 11/18/2022] Open
Abstract
The underlying genetic mechanisms affecting turkey growth traits have not been widely investigated. Genome-wide association studies (GWAS) is a powerful approach to identify candidate regions associated with complex phenotypes and diseases in livestock. In the present study, we performed GWAS to identify regions associated with 18-week body weight in a turkey population. The data included body weight observations for 24,989 female turkeys genotyped based on a 65K SNP panel. The analysis was carried out using a univariate mixed linear model with hatch-week-year and the 2 top principal components fitted as fixed effects and the accumulated polygenic effect of all markers captured by the genomic relationship matrix as random. Thirty-three significant markers were observed on 1, 2, 3, 4, 7 and 12 chromosomes, while 26 showed strong linkage disequilibrium extending up to 410 kb. These significant markers were mapped to 37 genes, of which 13 were novel. Interestingly, many of the investigated genes are known to be involved in growth and body weight. For instance, genes AKR1D1, PARP12, BOC, NCOA1, ADCY3 and CHCHD7 regulate growth, body weight, metabolism, digestion, bile acid biosynthetic and development of muscle cells. In summary, the results of our study revealed novel candidate genomic regions and candidate genes that could be managed within a turkey breeding program and adapted in fine mapping of quantitative trait loci to enhance genetic improvement in this species.
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Affiliation(s)
- Emhimad A. E. Abdalla
- Centre for Genetic Improvement of Livestock, University of Guelph, Guelph, Ontario, Canada
| | - Bayode O. Makanjuola
- Centre for Genetic Improvement of Livestock, University of Guelph, Guelph, Ontario, Canada
| | - Benjamin J. Wood
- Centre for Genetic Improvement of Livestock, University of Guelph, Guelph, Ontario, Canada
- School of Veterinary Science, University of Queensland, Gatton, Queensland, Australia
- Hybrid Turkeys, C-650 Riverbend Drive, Suite C, Kitchener, Canada
| | - Christine F. Baes
- Centre for Genetic Improvement of Livestock, University of Guelph, Guelph, Ontario, Canada
- Institute of Genetics, Vetsuisse Faculty, University of Bern, Bern, Switzerland
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25
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Flores RA, Cammayo PLT, Nguyen BT, Fernandez-Colorado CP, Kim S, Kim WH, Min W. Duck Interleukin-22: Identification and Expression Analysis in Riemerella anatipestifer Infection. J Immunol Res 2021; 2021:3862492. [PMID: 34805416 PMCID: PMC8601822 DOI: 10.1155/2021/3862492] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/10/2021] [Accepted: 10/07/2021] [Indexed: 01/05/2023] Open
Abstract
Riemerella anatipestifer is one of the most devastating pathogens affecting the global duck farms. Infection is involved in secretion of proinflammatory cytokines, including interleukin- (IL-) 17A. During the immune response to infection, IL-22 and IL-17A are often produced concurrently and at high levels in inflamed tissues. Little is known about duck IL-22 (duIL-22) during R. anatipestifer infection. We describe the characterization of duIL-22 and its mRNA expression analysis in splenic lymphocytes and macrophages treated with heat-killed R. anatipestifer and in the spleens and livers of R. anatipestifer-infected ducks. Full-length cDNA of duIL-22 encoded 197 amino acids. The deduced amino acid sequence of duIL-22 shared a 30.4-40.5% similarity with piscine counterparts, 57.4-60.1% with mammalian homologs, and 93.4% similarity to the chicken. Duck IL-22 mRNA expression level was relatively high in the skin of normal ducks. It was increased in mitogen-stimulated splenic lymphocytes and in killed R. anatipestifer-activated splenic lymphocytes and macrophages. Compared with healthy ducks, IL-22 transcript expression was significantly upregulated in the livers and spleens on days 1 and 4 postinfection, but not on day 7. IL-17A was significantly increased in the spleens only on day 4 postinfection and in the livers at all time points. When splenic lymphocytes were stimulated with heat-killed R. anatipestifer, CD4+ cells predominantly produced IL-22 while IL-17A was expressed both by CD4+ and CD4- cells. These results suggested that IL-22 and IL-17A are likely expressed in different cell types during R. anatipestifer infection.
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Affiliation(s)
- Rochelle A. Flores
- College of Veterinary Medicine & Institute of Animal Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea
| | - Paula Leona T. Cammayo
- College of Veterinary Medicine & Institute of Animal Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea
| | - Binh T. Nguyen
- College of Veterinary Medicine & Institute of Animal Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea
| | - Cherry P. Fernandez-Colorado
- Department of Veterinary Paraclinical Sciences, College of Veterinary Medicine, University of the Philippines Los Baños College, Laguna 4031, Philippines
| | - Suk Kim
- College of Veterinary Medicine & Institute of Animal Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea
| | - Woo H. Kim
- College of Veterinary Medicine & Institute of Animal Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea
| | - Wongi Min
- College of Veterinary Medicine & Institute of Animal Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea
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26
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Shnaf ASMA, Al-Khalifa MS. First constitutive heterochromatin characterization and Karyotype of white stork Ciconia ciconia (Aves: Ciconiidae). BRAZ J BIOL 2021; 83:e248814. [PMID: 34550286 DOI: 10.1590/1519-6984.248814] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/16/2021] [Accepted: 04/27/2021] [Indexed: 11/22/2022] Open
Abstract
The karyotype and constitutive heterochromatin pattern of the white stork Ciconia ciconia samples obtained from Manzala lake, Dimiaat, Egypt was described. Somatic cells of Ciconia ciconia samples have diploid number 2n= 68 chromosomes. Out of 68 chromosomes, 11 pairs including sex chromosomes were macrochromosomes and the remaining pairs were microchromosomes. Of the 11 macrochromosome pairs, no.1, 2, 4 and 5 were submetacentric and pairs no. 6, 7 and 8 were described as metacentric. In addition, the autosome pair no.3 was subtelocentric, while autosome pair no.9 was acrocentric. Also, the sex chromosome Z represents the fourth one in size and it was classified as submetacentric while, W chromosome appeared as medium size and was acrocentric. Furthermore, C-banding pattern (constitutive heterochromatin) revealed variation in their sizes and occurrence between macrochromosomes. Pairs no. 7 and 8 of autosomes exhibited unusual distribution of heterochromatin, where they appeared as entirely heterochromatic. This may be related to the origin of sex chromosomes Z and W. However, there is no sufficient evidence illustrate the appearance of entirely heterochromatic autosomes. Therefore, there is no available cytogenetic literature that describes the C-banding and karyotype of Ciconia Ciconia, so the results herein are important and may assist in cytogenetic study and evolutionary pattern of Ciconiiformes.
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Affiliation(s)
- A S M Abu Shnaf
- Minia University, Faculty of Science, Department of Zoology and Entomology, Minia, Egypt
| | - M S Al-Khalifa
- King Saud University, College of Science, Department of Zoology, Riyadh, Saudi Arabia
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27
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Investigating inbreeding in the turkey (Meleagris gallopavo) genome. Poult Sci 2021; 100:101366. [PMID: 34525446 PMCID: PMC8445901 DOI: 10.1016/j.psj.2021.101366] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/20/2021] [Revised: 06/02/2021] [Accepted: 06/24/2021] [Indexed: 02/06/2023] Open
Abstract
The detrimental effects of increased homozygosity due to inbreeding have prompted the development of methods to reduce inbreeding. The detection of runs of homozygosity (ROH), or contiguous stretches of homozygous marker genotypes, can be used to describe and quantify the level of inbreeding in an individual. The estimation of inbreeding coefficients can be calculated based on pedigree information, ROH, or the genomic relationship matrix. The aim of this study was to detect and describe ROH in the turkey genome and compare estimates of pedigree-based inbreeding coefficients (FPED) with genomic-based inbreeding coefficients estimated from ROH (FROH) and the genomic relationship matrix (FGRM). A total of 2,616,890 pedigree records were available. Of these records, 6,371 genotyped animals from three purebred turkey (Meleagris gallopavo) lines between 2013 and 2019 were available, and these were obtained using a dense single nucleotide polymorphism array (56,452 SNPs). The overall mean length of detected ROH was 2.87 ± 0.29 Mb with a mean number of 84.87 ± 8.79 ROH per animal. Short ROH with lengths of 1 to 2 Mb long were the most abundant throughout the genome. Mean ROH coverage differed greatly between chromosomes and lines. Considering inbreeding coefficient means across all lines, genomic derived inbreeding coefficients (FROH = 0.27; FGRM = 0.32) were higher than coefficients estimated from pedigree records (FPED = 0.14). Correlations between FROH and FPED, FROH and FGRM, and FPED and FGRM ranged between 0.19 to 0.31, 0.68 to 0.73, and 0.17 to 0.30, respectively. Additionally, correlations between FROH from different lengths and FPED substantially increased with ROH length from -0.06 to 0.33. Results of the current research, including the distribution of ROH throughout the genome and ROH-derived inbreeding estimates, can provide a more comprehensive description of inbreeding in the turkey genome. This knowledge can be used to evaluate genetic diversity, a requirement for genetic improvement, and develop methods to minimize inbreeding in turkey breeding programs.
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28
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Shen QK, Peng MS, Adeola AC, Kui L, Duan S, Miao YW, Eltayeb NM, Lichoti JK, Otecko NO, Strillacci MG, Gorla E, Bagnato A, Charles OS, Sanke OJ, Dawuda PM, Okeyoyin AO, Musina J, Njoroge P, Agwanda B, Kusza S, Nanaei HA, Pedar R, Xu MM, Du Y, Nneji LM, Murphy RW, Wang MS, Esmailizadeh A, Dong Y, Ommeh SC, Zhang YP. Genomic Analyses of Unveil Helmeted Guinea Fowl (Numida meleagris) Domestication in West Africa. Genome Biol Evol 2021; 13:6261762. [PMID: 34009300 PMCID: PMC8214406 DOI: 10.1093/gbe/evab090] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 04/30/2021] [Indexed: 12/22/2022] Open
Abstract
Domestication of the helmeted guinea fowl (HGF; Numida meleagris) in Africa remains elusive. Here we report a high-quality de novo genome assembly for domestic HGF generated by long- and short-reads sequencing together with optical and chromatin interaction mapping. Using this assembly as the reference, we performed population genomic analyses for newly sequenced whole-genomes for 129 birds from Africa, Asia, and Europe, including domestic animals (n = 89), wild progenitors (n = 34), and their closely related wild species (n = 6). Our results reveal domestication of HGF in West Africa around 1,300-5,500 years ago. Scanning for selective signals characterized the functional genes in behavior and locomotion changes involved in domestication of HGF. The pleiotropy and linkage in genes affecting plumage color and fertility were revealed in the recent breeding of Italian domestic HGF. In addition to presenting a missing piece to the jigsaw puzzle of domestication in poultry, our study provides valuable genetic resources for researchers and breeders to improve production in this species.
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Affiliation(s)
- Quan-Kuan Shen
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Sino-Africa Joint Research Center, Chinese Academy of Sciences, Nairobi, Kenya.,Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, China
| | - Min-Sheng Peng
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Sino-Africa Joint Research Center, Chinese Academy of Sciences, Nairobi, Kenya.,Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, China
| | - Adeniyi C Adeola
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Sino-Africa Joint Research Center, Chinese Academy of Sciences, Nairobi, Kenya.,Centre for Biotechnology Research, Bayero University, Kano, Nigeria
| | - Ling Kui
- Dana-Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts, USA
| | | | - Yong-Wang Miao
- Faculty of Animal Science and Technology, Yunnan Agricultural University, Kunming, China
| | - Nada M Eltayeb
- Department of Animal breeding and Reproduction Technology, College of Animal Production, University of Bahri, Khartoum, Sudan
| | - Jacqueline K Lichoti
- State Department of Livestock, Ministry of Agriculture Livestock Fisheries and Irrigation, Nairobi, Kenya
| | - Newton O Otecko
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Sino-Africa Joint Research Center, Chinese Academy of Sciences, Nairobi, Kenya.,Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, China
| | | | - Erica Gorla
- Department of Veterinary Medicine, Università degli Studi di Milano, Italy
| | - Alessandro Bagnato
- Department of Veterinary Medicine, Università degli Studi di Milano, Italy
| | | | - Oscar J Sanke
- Taraba State Ministry of Agriculture and Natural Resources, Jalingo, Nigeria
| | - Philip M Dawuda
- Department of Veterinary Surgery and Theriogenology, College of Veterinary Medicine, University of Agriculture, Makurdi, Nigeria
| | - Agboola O Okeyoyin
- National Park Service Headquarter, Federal Capital Territory, Abuja, Nigeria
| | - John Musina
- Department of Zoology, National Museums of Kenya, Nairobi, Kenya
| | - Peter Njoroge
- Department of Zoology, National Museums of Kenya, Nairobi, Kenya
| | - Bernard Agwanda
- Department of Zoology, National Museums of Kenya, Nairobi, Kenya
| | - Szilvia Kusza
- Centre for Agricultural Genomics and Biotechnology, University of Debrecen, Debrecen, Hungary
| | | | - Rana Pedar
- Department of Animal Science, Faculty of Agriculture, Shahid Bahonar University of Kerman, Iran
| | - Ming-Min Xu
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Sino-Africa Joint Research Center, Chinese Academy of Sciences, Nairobi, Kenya.,Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, China
| | - Yuan Du
- Nowbio Biotechnology Company, Kunming, China
| | - Lotanna M Nneji
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Sino-Africa Joint Research Center, Chinese Academy of Sciences, Nairobi, Kenya
| | - Robert W Murphy
- Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, Toronto, Ontario, Canada
| | - Ming-Shan Wang
- Howard Hughes Medical Institute, University of California Santa Cruz, California, USA.,Department of Ecology and Evolutionary Biology, University of California Santa Cruz, California, USA
| | - Ali Esmailizadeh
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Department of Animal Science, Faculty of Agriculture, Shahid Bahonar University of Kerman, Iran
| | - Yang Dong
- College of Biological Big Data, Yunnan Agriculture University, Kunming, China.,State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, China.,Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural University, Kunming, China
| | - Sheila C Ommeh
- Department of Zoology, National Museums of Kenya, Nairobi, Kenya.,Institute of Biotechnology Research, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya
| | - Ya-Ping Zhang
- State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.,Sino-Africa Joint Research Center, Chinese Academy of Sciences, Nairobi, Kenya.,Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, China.,State Key Laboratory for Conservation and Utilization of Bio-Resource in Yunnan, Yunnan University, Kunming, China.,Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China
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29
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Recuerda M, Vizueta J, Cuevas-Caballé C, Blanco G, Rozas J, Milá B. Chromosome-Level Genome Assembly of the Common Chaffinch (Aves: Fringilla coelebs): A Valuable Resource for Evolutionary Biology. Genome Biol Evol 2021; 13:evab034. [PMID: 33616654 PMCID: PMC8046334 DOI: 10.1093/gbe/evab034] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 02/16/2021] [Indexed: 12/26/2022] Open
Abstract
The common chaffinch, Fringilla coelebs, is one of the most common, widespread, and well-studied passerines in Europe, with a broad distribution encompassing Western Europe and parts of Asia, North Africa, and the Macaronesian archipelagos. We present a high-quality genome assembly of the common chaffinch generated using Illumina shotgun sequencing in combination with Chicago and Hi-C libraries. The final genome is a 994.87-Mb chromosome-level assembly, with 98% of the sequence data located in chromosome scaffolds and a N50 statistic of 69.73 Mb. Our genome assembly shows high completeness, with a complete BUSCO score of 93.9% using the avian data set. Around 7.8% of the genome contains interspersed repetitive elements. The structural annotation yielded 17,703 genes, 86.5% of which have a functional annotation, including 7,827 complete universal single-copy orthologs out of 8,338 genes represented in the BUSCO avian data set. This new annotated genome assembly will be a valuable resource as a reference for comparative and population genomic analyses of passerine, avian, and vertebrate evolution.
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Affiliation(s)
- María Recuerda
- National Museum of Natural Sciences, Spanish National Research Council (CSIC), Madrid, Spain
| | - Joel Vizueta
- National Museum of Natural Sciences, Spanish National Research Council (CSIC), Madrid, Spain
- Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
| | - Cristian Cuevas-Caballé
- Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
| | - Guillermo Blanco
- National Museum of Natural Sciences, Spanish National Research Council (CSIC), Madrid, Spain
| | - Julio Rozas
- Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
| | - Borja Milá
- National Museum of Natural Sciences, Spanish National Research Council (CSIC), Madrid, Spain
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30
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An interplay between compositional constraint and natural selection dictates the codon usage pattern among select Galliformes. Biosystems 2021; 204:104390. [PMID: 33636205 DOI: 10.1016/j.biosystems.2021.104390] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/28/2021] [Accepted: 02/18/2021] [Indexed: 11/20/2022]
Abstract
Galliformes are believed to be the first avian order that started living in human association and became domesticated. Members of this order ranged from common to rare species. Next-generation sequencing has availed researchers with the whole genome sequences of five Galliformes; chicken, helmeted Guinea fowl, turkey, Japanese quail, and peafowl. Bioinformatic analysis based on codon usage, evolution, and species-specific functional enrichment can provide some crucial information aiding proper understanding of their genomic strategies. In this study, we investigated the genomic features of chicken, helmeted guinea fowl, turkey, and Japanese quail. Their genomes were AT biased although the potentially highly expressed genes contained more GC than AT. Cytosine dominated the third position of frequently used optimal codons. Mutational pressures in the analyzed Galliformes were in the range of 0.2-0.6%. Neutrality plot, translational selection index, and mutational responsive index indicated the dominance of selection pressure over mutational pressure among Galliformes. A pair of di-nucleotides, TpA and CpG, was found to be used less frequently than others in protein-coding genes since both of them are associated with the conversion of euchromatin to heterochromatin. Functional enrichment analysis revealed the dominance of proteins associated with fundamental biological processes. In turkey, chicken and helmeted Guinea fowl proteins with immunity-boosting capacity prevailed along with proteins needed for signal transduction and maintenance of central dogma. Evolutionary analysis indicated a bias towards synonymous substitution than non-synonymous mutation.
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31
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Jaiswal SK, Gupta A, Shafer ABA, P. K. VP, Vijay N, Sharma VK. Genomic Insights Into the Molecular Basis of Sexual Selection in Birds. Front Ecol Evol 2021. [DOI: 10.3389/fevo.2021.538498] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/13/2022] Open
Abstract
Sexual selection is a well-known biological process, yet the genomic basis and patterns of sexual selection are not fully understood. The extravagant ornamental plumage of peacock (Pavo cristatus) was instrumental in shaping Charles Darwin's theory of sexual selection and is considered to be an honest signal of its immunocompetence. Here, we used the recently generated draft genome sequence of peafowl (Pavo cristatus) and carried out a comparative analysis across 11 bird genomes that encompass a range of sexual selection and also had high-quality genomic and phenotypic data publically available to study the genomic basis of sexual selection. We found that varying degree of purifying selection was the predominant mechanism of action for sexual selection at the genome-wide scale and observed that sexual selection mostly influences genes regulating gene expression and protein processing. Specifically, the genome-wide phylogenetically corrected regression analysis supported the continuous or ongoing model of sexual selection. Genes involved in nucleic acid binding and gene expression regulation, including a specific regulator of sex-determination known as TRA2A to be under positive selection in the species with high post-copulatory sexual selection manifested as high sperm competition. We also detected specific feather-related and immune-related gene-pairs evolving under similar selection pressures across the 11 species, including peacock (Pavo cristatus), which is consistent with the Hamilton-Zuk hypothesis. The comparative genomics analysis of 11 avian taxa has provided new insights on the molecular underpinnings of sexual selection and identifies specific genomic regions for future in-depth analysis.
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32
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Zimmerman SJ, Aldridge CL, Langin KM, Wann GT, Scott Cornman R, Oyler-McCance SJ. Environmental gradients of selection for an alpine-obligate bird, the white-tailed ptarmigan (Lagopus leucura). Heredity (Edinb) 2021; 126:117-131. [PMID: 32807852 PMCID: PMC7852610 DOI: 10.1038/s41437-020-0352-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/28/2020] [Revised: 07/27/2020] [Accepted: 07/28/2020] [Indexed: 11/08/2022] Open
Abstract
The warming climate will expose alpine species adapted to a highly seasonal, harsh environment to novel environmental conditions. A species can shift their distribution, acclimate, or adapt in response to a new climate. Alpine species have little suitable habitat to shift their distribution, and the limits of acclimation will likely be tested by climate change in the long-term. Adaptive genetic variation may provide the raw material for species to adapt to this changing environment. Here, we use a genomic approach to describe adaptive divergence in an alpine-obligate species, the white-tailed ptarmigan (Lagopus leucura), a species distributed from Alaska to New Mexico, across an environmentally variable geographic range. Previous work has identified genetic structure and morphological, behavioral, and physiological differences across the species' range; however, those studies were unable to determine the degree to which adaptive divergence is correlated with local variation in environmental conditions. We used a genome-wide dataset generated from 95 white-tailed ptarmigan distributed throughout the species' range and genotype-environment association analyses to identify the genetic signature and environmental drivers of local adaptation. We detected associations between multiple environmental gradients and candidate adaptive loci, suggesting ptarmigan populations may be locally adapted to the plant community composition, elevation, local climate, and to the seasonality of the environment. Overall, our results suggest there may be groups within the species' range with genetic variation that could be essential for adapting to a changing climate and helpful in guiding conservation action.
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Affiliation(s)
- Shawna J Zimmerman
- U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg. C, Fort Collins, CO, 80526, USA.
| | - Cameron L Aldridge
- U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg. C, Fort Collins, CO, 80526, USA
| | - Kathryn M Langin
- U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg. C, Fort Collins, CO, 80526, USA
| | - Gregory T Wann
- U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg. C, Fort Collins, CO, 80526, USA
| | - R Scott Cornman
- U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg. C, Fort Collins, CO, 80526, USA
| | - Sara J Oyler-McCance
- U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg. C, Fort Collins, CO, 80526, USA
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33
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Monson MS, Bearson BL, Sylte MJ, Looft T, Lamont SJ, Bearson SMD. Transcriptional response of blood leukocytes from turkeys challenged with Salmonella enterica serovar Typhimurium UK1. Vet Immunol Immunopathol 2020; 232:110181. [PMID: 33401108 DOI: 10.1016/j.vetimm.2020.110181] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/05/2020] [Revised: 12/14/2020] [Accepted: 12/21/2020] [Indexed: 12/25/2022]
Abstract
Non-typhoidal Salmonella is one of the most common causes of bacterial foodborne disease and consumption of contaminated poultry products, including turkey, is one source of exposure. Minimizing Salmonella colonization of commercial turkeys could decrease the incidence of Salmonella-associated human foodborne illness. Understanding host responses to these bacteria is critical in developing strategies to minimize colonization and reduce food safety risk. In this study, we evaluated bacterial load and blood leukocyte transcriptomic responses of 3-week-old turkeys challenged with the Salmonella enterica serovar Typhimurium (S. Typhimurium) UK1 strain. Turkeys (n = 8/dose) were inoculated by oral gavage with 108 or 1010 colony forming units (CFU) of S. Typhimurium UK1, and fecal shedding and tissue colonization were measured across multiple days post-inoculation (dpi). Fecal shedding was 1-2 log10 higher in the 1010 CFU group than the 108 CFU group, but both doses effectively colonized the crop, spleen, ileum, cecum, colon, bursa of Fabricius and cloaca without causing any detectable clinical signs in either group of birds. Blood leukocytes were isolated from a subset of the birds (n = 3-4/dpi) both pre-inoculation (0 dpi) and 2 dpi with 1010 CFU and their transcriptomic responses assayed by RNA-sequencing (RNA-seq). At 2 dpi, 647 genes had significant differential expression (DE), including large increases in expression of immune genes such as CCAH221, IL4I1, LYZ, IL13RA2, IL22RA2, and ACOD1. IL1β was predicted as a major regulator of DE in the leukocytes, which was predicted to activate cell migration, phagocytosis and proliferation, and to impact the STAT3 and toll-like receptor pathways. These analyses revealed genes and pathways by which turkey blood leukocytes responded to the pathogen and can provide potential targets for developing intervention strategies or diagnostic assays to mitigate S. Typhimurium colonization in turkeys.
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Affiliation(s)
- Melissa S Monson
- Iowa State University, Department of Animal Science, Ames, IA, United States
| | - Bradley L Bearson
- USDA, ARS, National Laboratory for Agriculture and the Environment, Ames, IA, United States
| | - Matthew J Sylte
- USDA, ARS, National Animal Disease Center, Ames, IA, United States
| | - Torey Looft
- USDA, ARS, National Animal Disease Center, Ames, IA, United States
| | - Susan J Lamont
- Iowa State University, Department of Animal Science, Ames, IA, United States
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High-Density Linkage Maps Based on Genotyping-by-Sequencing (GBS) Confirm a Chromosome-Level Genome Assembly and Reveal Variation in Recombination Rate for the Pacific Oyster Crassostrea gigas. G3-GENES GENOMES GENETICS 2020; 10:4691-4705. [PMID: 33144392 PMCID: PMC7718752 DOI: 10.1534/g3.120.401728] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
Abstract
Studies of linkage and linkage mapping have advanced genetic and biological knowledge for over 100 years. In addition to their growing role, today, in mapping phenotypes to genotypes, dense linkage maps can help to validate genome assemblies. Previously, we showed that 40% of scaffolds in the first genome assembly for the Pacific oyster Crassostrea gigas were chimeric, containing single nucleotide polymorphisms (SNPs) mapping to different linkage groups. Here, we merge 14 linkage maps constructed of SNPs generated from genotyping-by-sequencing (GBS) methods with five, previously constructed linkage maps, to create a compendium of nearly 69 thousand SNPs mapped with high confidence. We use this compendium to assess a recently available, chromosome-level assembly of the C. gigas genome, mapping SNPs in 275 of 301 contigs and comparing the ordering of these contigs, by linkage, to their assembly by Hi-C sequencing methods. We find that, while 26% of contigs contain chimeric blocks of SNPs, i.e., adjacent SNPs mapping to different linkage groups than the majority of SNPs in their contig, these apparent misassemblies amount to only 0.08% of the genome sequence. Furthermore, nearly 90% of 275 contigs mapped by linkage and sequencing are assembled identically; inconsistencies between the two assemblies for the remaining 10% of contigs appear to result from insufficient linkage information. Thus, our compilation of linkage maps strongly supports this chromosome-level assembly of the oyster genome. Finally, we use this assembly to estimate, for the first time in a Lophotrochozoan, genome-wide recombination rates and causes of variation in this fundamental process.
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He C, Zhao L, Xiao L, Xu K, Ding J, Zhou H, Zheng Y, Han C, Akinyemi F, Luo H, Yang L, Luo L, Yuan H, Lu X, Meng H. Chromosome level assembly reveals a unique immune gene organization and signatures of evolution in the common pheasant. Mol Ecol Resour 2020; 21:897-911. [PMID: 33188724 DOI: 10.1111/1755-0998.13296] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/09/2020] [Revised: 11/03/2020] [Accepted: 11/06/2020] [Indexed: 12/30/2022]
Abstract
The common pheasant Phasianus colchicus, belonging to the order Galliformes and family Phasianidae, is the most widespread species. Despite a long history of captivity, the domestication of this bird is still at a preliminary stage. Recently, the demand for accelerating its transformation to poultry for meat and egg production has been increasing. In this study, we assembled high quality, chromosome scale genome of the common pheasant by using PacBio long reads, next-generation short reads, and Hi-C technology. The primary assembly has contig N50 size of 1.33 Mb and scaffold N50 size of 59.46 Mb, with a total size of 0.99 Gb, resolving most macrochromosomes into single scaffolds. A total of 23,058 genes and 10.71 Mb interspersed repeats were identified, constituting 30.31% and 10.71% of the common pheasant genome, respectively. Our phylogenetic analysis revealed that the common pheasant shared common ancestors with turkey about 24.7-34.5 million years ago (Ma). Rapidly evolved gene families, as well as branch-specific positively selected genes, indicate that calcium-related genes are potentially related to the adaptive and evolutionary change of the common pheasant. Interestingly, we found that the common pheasant has a unique major histocompatibility complex B locus (MHC-B) structure: three major inversions occurred in the sequence compared with chicken MHC-B. Furthermore, we detected signals of selection in five breeds of domestic common pheasant, several of which are production-oriented.
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Affiliation(s)
- Chuan He
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Lele Zhao
- Shanghai Animal Disease Control Center, Shanghai, China
| | - Lu Xiao
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Ke Xu
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Jinmei Ding
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Hao Zhou
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Yuming Zheng
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Chengxiao Han
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Fisayo Akinyemi
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Huaixi Luo
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Lingyu Yang
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Lingxiao Luo
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
| | - Hongyan Yuan
- Shanghai Xinhao Rare Poultry Breeding Co. Ltd., Shanghai, China
| | - Xuelin Lu
- Shanghai Animal Disease Control Center, Shanghai, China
| | - He Meng
- Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
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Abdalla EA, Id‐Lahoucine S, Cánovas A, Casellas J, Schenkel FS, Wood BJ, Baes CF. Discovering lethal alleles across the turkey genome using a transmission ratio distortion approach. Anim Genet 2020; 51:876-889. [PMID: 33006154 PMCID: PMC7702127 DOI: 10.1111/age.13003] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 08/28/2020] [Indexed: 12/23/2022]
Abstract
Deviation from Mendelian inheritance expectations (transmission ratio distortion, TRD) has been observed in several species, including the mouse and humans. In this study, TRD was characterized in the turkey genome using both allelic (specific- and unspecific-parent TRD) and genotypic (additive- and dominance-TRD) parameterizations within a Bayesian framework. In this study, we evaluated TRD for 23 243 genotyped Turkeys across 56 393 autosomal SNPs. The analyses included 500 sires, 2013 dams and 11 047 offspring (trios). Three different haplotype sliding windows of 4, 10 and 20 SNPs were used across the autosomal chromosomes. Based on the genotypic parameterizations, 14 haplotypes showed additive and dominance TRD effects highlighting regions with a recessive TRD pattern. In contrast, the allelic model uncovered 12 haplotype alleles with the allelic TRD pattern which showed an underrepresentation of heterozygous offspring in addition to the absence of homozygous animals. For regions with the allelic pattern, only one particular region showed a parent-specific TRD where the penetrance was high via the dam, but low via the sire. The gene set analysis uncovered several gene ontology functional terms, Reactome pathways and several Medical Subject Headings that showed significant enrichment of genes associated with TRD. Many of these gene ontology functional terms (e.g. mitotic spindle assembly checkpoint, DRM complex and Aneuploidy), Reactome pathways (e.g. Mismatch repair) and Medical Subject Headings (e.g. Adenosine monophosphate) are known to be related to fertility, embryo development and lethality. The results of this study revealed potential novel candidate lethal haplotypes, functional terms and pathways that may enhance breeding programs in Turkeys through reducing mortality and improving reproduction rate.
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Affiliation(s)
- E. A. Abdalla
- Centre for Genetic Improvement of Livestock, Department of Animal BiosciencesUniversity of GuelphGuelphONN1G 2W1Canada
| | - S. Id‐Lahoucine
- Centre for Genetic Improvement of Livestock, Department of Animal BiosciencesUniversity of GuelphGuelphONN1G 2W1Canada
| | - A. Cánovas
- Centre for Genetic Improvement of Livestock, Department of Animal BiosciencesUniversity of GuelphGuelphONN1G 2W1Canada
| | - J. Casellas
- Departament de Ciència Animal i dels AlimentsUniversitat Autònoma de BarcelonaBellaterra08193Spain
| | - F. S. Schenkel
- Centre for Genetic Improvement of Livestock, Department of Animal BiosciencesUniversity of GuelphGuelphONN1G 2W1Canada
| | - B. J. Wood
- Centre for Genetic Improvement of Livestock, Department of Animal BiosciencesUniversity of GuelphGuelphONN1G 2W1Canada
- Hybrid TurkeysC‐650 Riverbend Drive, Suite CKitchenerONN2K 3S2Canada
- School of Veterinary ScienceUniversity of QueenslandGattonQld4343Australia
| | - C. F. Baes
- Centre for Genetic Improvement of Livestock, Department of Animal BiosciencesUniversity of GuelphGuelphONN1G 2W1Canada
- Institute of Genetics, Vetsuisse FacultyUniversity of BernBern3001Switzerland
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Marín I. Tumor Necrosis Factor Superfamily: Ancestral Functions and Remodeling in Early Vertebrate Evolution. Genome Biol Evol 2020; 12:2074-2092. [PMID: 33210144 PMCID: PMC7674686 DOI: 10.1093/gbe/evaa140] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 06/29/2020] [Indexed: 01/01/2023] Open
Abstract
The evolution of the tumor necrosis factor superfamily (TNFSF) in early vertebrates is inferred by comparing the TNFSF genes found in humans and nine fishes: three agnathans, two chondrichthyans, three actinopterygians, and the sarcopterygian Latimeria chalumnae. By combining phylogenetic and synteny analyses, the TNFSF sequences detected are classified into five clusters of genes and 24 orthology groups. A model for their evolution since the origin of vertebrates is proposed. Fifteen TNFSF genes emerged from just three progenitors due to the whole-genome duplications (WGDs) that occurred before the agnathan/gnathostome split. Later, gnathostomes not only kept most of the genes emerged in the WGDs but soon added several tandem duplicates. More recently, complex, lineage-specific patterns of duplications and losses occurred in different gnathostome lineages. In agnathan species only seven to eight TNFSF genes are detected, because this lineage soon lost six of the genes emerged in the ancestral WGDs and additional losses in both hagfishes and lampreys later occurred. The orthologs of many of these lost genes are, in mammals, ligands of death-domain-containing TNFSF receptors, indicating that the extrinsic apoptotic pathway became simplified in the agnathan lineage. From the patterns of emergence of these genes, it is deduced that both the regulation of apoptosis and the control of the NF-κB pathway that depends in modern mammals on TNFSF members emerged before the ancestral vertebrate WGDs.
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Affiliation(s)
- Ignacio Marín
- Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Científicas (IBV-CSIC), Valencia, Spain
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38
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Zhou C, Liu Y, Qiao L, Liu Y, Yang N, Meng Y, Yue B. The draft genome of the blood pheasant ( Ithaginis cruentus): Phylogeny and high-altitude adaptation. Ecol Evol 2020; 10:11440-11452. [PMID: 33144976 PMCID: PMC7593199 DOI: 10.1002/ece3.6782] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/12/2020] [Revised: 06/30/2020] [Accepted: 08/20/2020] [Indexed: 11/10/2022] Open
Abstract
The blood pheasant (Ithaginis cruentus), the only species in the genus Ithaginis, lives in an extremely inhospitable high-altitude environment, coping with hypoxia and ultraviolet (UV) radiation. To further investigate the phylogeny of Phasianidae species based on complete genomes and understand the molecular genetic mechanisms of the high-altitude adaptation of the blood pheasant, we de novo assembled and annotated the complete genome of the blood pheasant. The blood pheasant genome size is 1.04 Gb with scaffold N50 of 10.88 Mb. We identified 109.92 Mb (10.62%) repetitive elements, 279,037 perfect microsatellites, and 17,209 protein-coding genes. The phylogenetic tree of Phasianidae based on whole genomes revealed three highly supported major clades with the blood pheasant included in the "erectile clade." Comparative genomics analysis showed that many genes were positively selected in the blood pheasant, which was associated with response to hypoxia and/or UV radiation. More importantly, among these positively selected genes (PSGs) which were related to high-altitude adaptation, sixteen PSGs had blood pheasant-specific missense mutations. Our data and analysis lay solid foundation to the study of Phasianidae phylogeny and provided new insights into the potential adaptation mechanisms to the high altitude employed by the blood pheasant.
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Affiliation(s)
- Chuang Zhou
- Key Laboratory of Bioresources and Ecoenvironment (Ministry of Education)College of Life SciencesSichuan UniversityChengduChina
| | - Yi Liu
- Key Laboratory of Bioresources and Ecoenvironment (Ministry of Education)College of Life SciencesSichuan UniversityChengduChina
| | - Lu Qiao
- Key Laboratory of Bioresources and Ecoenvironment (Ministry of Education)College of Life SciencesSichuan UniversityChengduChina
| | - Yang Liu
- Chengdu Zoo/Chengdu Wildlife Research InstituteChengduChina
| | - Nan Yang
- Institute of Qinghai‐Tibetan PlateauSouthwest Minzu UniversityChengduChina
| | - Yang Meng
- Key Laboratory of Bioresources and Ecoenvironment (Ministry of Education)College of Life SciencesSichuan UniversityChengduChina
| | - Bisong Yue
- Key Laboratory of Bioresources and Ecoenvironment (Ministry of Education)College of Life SciencesSichuan UniversityChengduChina
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Groß C, Bortoluzzi C, de Ridder D, Megens HJ, Groenen MAM, Reinders M, Bosse M. Prioritizing sequence variants in conserved non-coding elements in the chicken genome using chCADD. PLoS Genet 2020; 16:e1009027. [PMID: 32966296 PMCID: PMC7535126 DOI: 10.1371/journal.pgen.1009027] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/18/2020] [Revised: 10/05/2020] [Accepted: 08/05/2020] [Indexed: 11/30/2022] Open
Abstract
The availability of genomes for many species has advanced our understanding of the non-protein-coding fraction of the genome. Comparative genomics has proven itself to be an invaluable approach for the systematic, genome-wide identification of conserved non-protein-coding elements (CNEs). However, for many non-mammalian model species, including chicken, our capability to interpret the functional importance of variants overlapping CNEs has been limited by current genomic annotations, which rely on a single information type (e.g. conservation). We here studied CNEs in chicken using a combination of population genomics and comparative genomics. To investigate the functional importance of variants found in CNEs we develop a ch(icken) Combined Annotation-Dependent Depletion (chCADD) model, a variant effect prediction tool first introduced for humans and later on for mouse and pig. We show that 73 Mb of the chicken genome has been conserved across more than 280 million years of vertebrate evolution. The vast majority of the conserved elements are in non-protein-coding regions, which display SNP densities and allele frequency distributions characteristic of genomic regions constrained by purifying selection. By annotating SNPs with the chCADD score we are able to pinpoint specific subregions of the CNEs to be of higher functional importance, as supported by SNPs found in these subregions are associated with known disease genes in humans, mice, and rats. Taken together, our findings indicate that CNEs harbor variants of functional significance that should be object of further investigation along with protein-coding mutations. We therefore anticipate chCADD to be of great use to the scientific community and breeding companies in future functional studies in chicken.
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Affiliation(s)
- Christian Groß
- Bioinformatics Group, Wageningen University & Research, 6708 PB, Wageningen, The Netherlands
- Delft Bioinformatics Lab, University of Technology Delft, 2600 GA, Delft, The Netherlands
| | - Chiara Bortoluzzi
- Animal Breeding and Genomics Group, Wageningen University & Research, 6708 PB, Wageningen, The Netherlands
| | - Dick de Ridder
- Bioinformatics Group, Wageningen University & Research, 6708 PB, Wageningen, The Netherlands
| | - Hendrik-Jan Megens
- Animal Breeding and Genomics Group, Wageningen University & Research, 6708 PB, Wageningen, The Netherlands
| | - Martien A. M. Groenen
- Animal Breeding and Genomics Group, Wageningen University & Research, 6708 PB, Wageningen, The Netherlands
| | - Marcel Reinders
- Delft Bioinformatics Lab, University of Technology Delft, 2600 GA, Delft, The Netherlands
| | - Mirte Bosse
- Animal Breeding and Genomics Group, Wageningen University & Research, 6708 PB, Wageningen, The Netherlands
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40
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Strillacci MG, Marelli SP, Martinez-Velazquez G. Hybrid Versus Autochthonous Turkey Populations: Homozygous Genomic Regions Occurrences Due to Artificial and Natural Selection. Animals (Basel) 2020; 10:ani10081318. [PMID: 32751760 PMCID: PMC7460020 DOI: 10.3390/ani10081318] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/15/2020] [Revised: 07/27/2020] [Accepted: 07/28/2020] [Indexed: 12/28/2022] Open
Abstract
Simple Summary In this study we investigate the genomic differentiation of traditional Mexican turkey breeds and commercial hybrid strains. The analysis aimed to identify the effects of different types of selection on the birds’ genome structure. Mexican turkeys are characterized by an adaptive selection to their specific original environment; on the other hand, commercial hybrid strains are directionally selected to maximize productive traits and to reduce production costs. The Mexican turkeys were grouped in two geographic subpopulations, while high genomic homogeneity was found in hybrid birds. Traditional breeds and commercial strains are clearly differentiated from a genetic point of view. Inbreeding coefficients were here calculated with different approaches. A clear effect of selection for productive traits was recorded. Abstract The Mexican turkey population is considered to be the descendant of the original domesticated wild turkey and it is distinct from hybrid strains obtained by the intense artificial selection activity that has occurred during the last 40 years. In this study 30 Mexican turkeys were genomically compared to 38 commercial hybrids using 327,342 SNP markers in order to elucidate the differences in genome variability resulting from different types of selection, i.e., only adaptive for Mexican turkey, and strongly directional for hybrids. Runs of homozygosity (ROH) were detected and the two inbreeding coefficients (F and FROH) based on genomic information were calculated. Principal component and admixture analyses revealed two different clusters for Mexican turkeys (MEX_cl_1 and MEX_cl_2) showing genetic differentiation from hybrids (HYB) (FST equal 0.168 and 0.167, respectively). A total of 3602 ROH were found in the genome of the all turkeys populations. ROH resulted mainly short in length and the ROH_island identified in HYB (n = 9), MEX_cl_1 (n = 1), and MEX_cl_2 (n = 2) include annotated genes related to production traits: abdominal fat (percentage and weight) and egg characteristics (egg shell color and yolk weight). F and FROH resulted correlated to each other only for Mexican populations. Mexican turkey genomic variability allows us to separate the birds into two subgroups according to the geographical origin of samples, while the genomic homogeneity of hybrid birds reflected the strong directional selection occurring in this population.
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Affiliation(s)
- Maria Giuseppina Strillacci
- Department of Veterinary Medicine, University of Milan, Via Festa del Perdono, 7, 20122 Milano, Italy;
- Correspondence: ; Tel.: +39-025-033-4582
| | - Stefano Paolo Marelli
- Department of Veterinary Medicine, University of Milan, Via Festa del Perdono, 7, 20122 Milano, Italy;
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Facciuolo A, Denomy C, Lipsit S, Kusalik A, Napper S. From Beef to Bees: High-Throughput Kinome Analysis to Understand Host Responses of Livestock Species to Infectious Diseases and Industry-Associated Stress. Front Immunol 2020; 11:765. [PMID: 32499776 PMCID: PMC7243914 DOI: 10.3389/fimmu.2020.00765] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/04/2020] [Accepted: 04/06/2020] [Indexed: 11/13/2022] Open
Abstract
Within human health research, the remarkable utility of kinase inhibitors as therapeutics has motivated efforts to understand biology at the level of global cellular kinase activity (the kinome). In contrast, the diminished potential for using kinase inhibitors in food animals has dampened efforts to translate this research approach to livestock species. This, in our opinion, was a lost opportunity for livestock researchers given the unique potential of kinome analysis to offer insight into complex biology. To remedy this situation, our lab developed user-friendly, cost-effective approaches for kinome analysis that can be readily incorporated into most research programs but with a specific priority to enable the technology to livestock researchers. These contributions include the development of custom software programs for the creation of species-specific kinome arrays as well as comprehensive deconvolution and analysis of kinome array data. Presented in this review are examples of the application of kinome analysis to highlight the utility of the technology to further our understanding of two key complex biological events of priority to the livestock industry: host immune responses to infectious diseases and animal stress responses. These advances and examples of application aim to provide both mechanisms and motivation for researchers, particularly livestock researchers, to incorporate kinome analysis into their research programs.
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Affiliation(s)
- Antonio Facciuolo
- Vaccine and Infectious Disease Organization - International Vaccine Centre, University of Saskatchewan, Saskatoon, SK, Canada
| | - Connor Denomy
- Vaccine and Infectious Disease Organization - International Vaccine Centre, University of Saskatchewan, Saskatoon, SK, Canada.,Department of Computer Science, University of Saskatchewan, Saskatoon, SK, Canada
| | - Sean Lipsit
- Vaccine and Infectious Disease Organization - International Vaccine Centre, University of Saskatchewan, Saskatoon, SK, Canada.,Department of Biochemistry, Microbiology and Immunology, University of Saskatchewan, Saskatoon, SK, Canada
| | - Anthony Kusalik
- Department of Computer Science, University of Saskatchewan, Saskatoon, SK, Canada
| | - Scott Napper
- Vaccine and Infectious Disease Organization - International Vaccine Centre, University of Saskatchewan, Saskatoon, SK, Canada.,Department of Biochemistry, Microbiology and Immunology, University of Saskatchewan, Saskatoon, SK, Canada
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Heimroth RD, Casadei E, Salinas I. Molecular Drivers of Lymphocyte Organization in Vertebrate Mucosal Surfaces: Revisiting the TNF Superfamily Hypothesis. JOURNAL OF IMMUNOLOGY (BALTIMORE, MD. : 1950) 2020; 204:2697-2711. [PMID: 32238457 PMCID: PMC7872792 DOI: 10.4049/jimmunol.1901059] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/30/2019] [Accepted: 02/26/2020] [Indexed: 12/19/2022]
Abstract
The adaptive immune system of all jawed vertebrates relies on the presence of B and T cell lymphocytes that aggregate in specific body sites to form primary and secondary lymphoid structures. Secondary lymphoid organs include organized MALT (O-MALT) such as the tonsils and Peyer patches. O-MALT became progressively organized during vertebrate evolution, and the TNF superfamily of genes has been identified as essential for the formation and maintenance of O-MALT and other secondary and tertiary lymphoid structures in mammals. Yet, the molecular drivers of O-MALT structures found in ectotherms and birds remain essentially unknown. In this study, we provide evidence that TNFSFs, such as lymphotoxins, are likely not a universal mechanism to maintain O-MALT structures in adulthood of teleost fish, sarcopterygian fish, or birds. Although a role for TNFSF2 (TNF-α) cannot be ruled out, transcriptomics suggest that maintenance of O-MALT in nonmammalian vertebrates relies on expression of diverse genes with shared biological functions in neuronal signaling. Importantly, we identify that expression of many genes with olfactory function is a unique feature of mammalian Peyer patches but not the O-MALT of birds or ectotherms. These results provide a new view of O-MALT evolution in vertebrates and indicate that different genes with shared biological functions may have driven the formation of these lymphoid structures by a process of convergent evolution.
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Affiliation(s)
- Ryan D Heimroth
- Center for Evolutionary and Theoretical Immunology, University of New Mexico, Albuquerque, NM 87131; and
- Department of Biology, University of New Mexico, Albuquerque, NM 87131
| | - Elisa Casadei
- Center for Evolutionary and Theoretical Immunology, University of New Mexico, Albuquerque, NM 87131; and
- Department of Biology, University of New Mexico, Albuquerque, NM 87131
| | - Irene Salinas
- Center for Evolutionary and Theoretical Immunology, University of New Mexico, Albuquerque, NM 87131; and
- Department of Biology, University of New Mexico, Albuquerque, NM 87131
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Steinegger M, Salzberg SL. Terminating contamination: large-scale search identifies more than 2,000,000 contaminated entries in GenBank. Genome Biol 2020; 21:115. [PMID: 32398145 PMCID: PMC7218494 DOI: 10.1186/s13059-020-02023-1] [Citation(s) in RCA: 126] [Impact Index Per Article: 25.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/27/2020] [Accepted: 04/16/2020] [Indexed: 12/20/2022] Open
Abstract
Genomic analyses are sensitive to contamination in public databases caused by incorrectly labeled reference sequences. Here, we describe Conterminator, an efficient method to detect and remove incorrectly labeled sequences by an exhaustive all-against-all sequence comparison. Our analysis reports contamination of 2,161,746, 114,035, and 14,148 sequences in the RefSeq, GenBank, and NR databases, respectively, spanning the whole range from draft to “complete” model organism genomes. Our method scales linearly with input size and can process 3.3 TB in 12 days on a 32-core computer. Conterminator can help ensure the quality of reference databases. Source code (GPLv3): https://github.com/martin-steinegger/conterminator
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Affiliation(s)
- Martin Steinegger
- School of Biological Sciences, Seoul National University, Seoul, 08826, South Korea. .,Center for Computational Biology, Whiting School of Engineering, Johns Hopkins University, Baltimore, 21218, Maryland, USA. .,Institute of Molecular Biology and Genetics, Seoul National University, Seoul, 08826, South Korea.
| | - Steven L Salzberg
- Center for Computational Biology, Whiting School of Engineering, Johns Hopkins University, Baltimore, 21218, Maryland, USA.,Department of Biomedical Engineering, Johns Hopkins University, Baltimore, 21218, Maryland, USA.,Departments of Computer Science and Biostatistics, Johns Hopkins University, Baltimore, 21218, Maryland, USA
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Hosseini M, Pratas D, Morgenstern B, Pinho AJ. Smash++: an alignment-free and memory-efficient tool to find genomic rearrangements. Gigascience 2020; 9:giaa048. [PMID: 32432328 PMCID: PMC7238676 DOI: 10.1093/gigascience/giaa048] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/11/2020] [Revised: 04/06/2020] [Accepted: 04/20/2020] [Indexed: 12/05/2022] Open
Abstract
BACKGROUND The development of high-throughput sequencing technologies and, as its result, the production of huge volumes of genomic data, has accelerated biological and medical research and discovery. Study on genomic rearrangements is crucial owing to their role in chromosomal evolution, genetic disorders, and cancer. RESULTS We present Smash++, an alignment-free and memory-efficient tool to find and visualize small- and large-scale genomic rearrangements between 2 DNA sequences. This computational solution extracts information contents of the 2 sequences, exploiting a data compression technique to find rearrangements. We also present Smash++ visualizer, a tool that allows the visualization of the detected rearrangements along with their self- and relative complexity, by generating an SVG (Scalable Vector Graphics) image. CONCLUSIONS Tested on several synthetic and real DNA sequences from bacteria, fungi, Aves, and Mammalia, the proposed tool was able to accurately find genomic rearrangements. The detected regions were in accordance with previous studies, which took alignment-based approaches or performed FISH (fluorescence in situ hybridization) analysis. The maximum peak memory usage among all experiments was ∼1 GB, which makes Smash++ feasible to run on present-day standard computers.
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Affiliation(s)
- Morteza Hosseini
- IEETA/DETI, University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
| | - Diogo Pratas
- IEETA/DETI, University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
- Department of Virology, University of Helsinki, Haartmaninkatu 3, 00014 Helsinki, Finland
| | - Burkhard Morgenstern
- Department of Bioinformatics, University of Göttingen, Goldschmidtstr. 1, 37077 Göttingen, Germany
- Göttingen Center of Molecular Biosciences (GZMB), Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
| | - Armando J Pinho
- IEETA/DETI, University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
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Wang W, Wang F, Hao R, Wang A, Sharshov K, Druzyaka A, Lancuo Z, Shi Y, Feng S. First de novo whole genome sequencing and assembly of the bar-headed goose. PeerJ 2020; 8:e8914. [PMID: 32292659 PMCID: PMC7144584 DOI: 10.7717/peerj.8914] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/23/2019] [Accepted: 03/15/2020] [Indexed: 12/23/2022] Open
Abstract
Background The bar-headed goose (Anser indicus) mainly inhabits the plateau wetlands of Asia. As a specialized high-altitude species, bar-headed geese can migrate between South and Central Asia and annually fly twice over the Himalayan mountains along the central Asian flyway. The physiological, biochemical and behavioral adaptations of bar-headed geese to high-altitude living and flying have raised much interest. However, to date, there is still no genome assembly information publicly available for bar-headed geese. Methods In this study, we present the first de novo whole genome sequencing and assembly of the bar-headed goose, along with gene prediction and annotation. Results 10X Genomics sequencing produced a total of 124 Gb sequencing data, which can cover the estimated genome size of bar-headed goose for 103 times (average coverage). The genome assembly comprised 10,528 scaffolds, with a total length of 1.143 Gb and a scaffold N50 of 10.09 Mb. Annotation of the bar-headed goose genome assembly identified a total of 102 Mb (8.9%) of repetitive sequences, 16,428 protein-coding genes, and 282 tRNAs. In total, we determined that there were 63 expanded and 20 contracted gene families in the bar-headed goose compared with the other 15 vertebrates. We also performed a positive selection analysis between the bar-headed goose and the closely related low-altitude goose, swan goose (Anser cygnoides), to uncover its genetic adaptations to the Qinghai-Tibetan Plateau. Conclusion We reported the currently most complete genome sequence of the bar-headed goose. Our assembly will provide a valuable resource to enhance further studies of the gene functions of bar-headed goose. The data will also be valuable for facilitating studies of the evolution, population genetics and high-altitude adaptations of the bar-headed geese at the genomic level.
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Affiliation(s)
- Wen Wang
- State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xi'ning, Qinghai, China
| | - Fang Wang
- Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xi'ning, Qinghai, China
| | - Rongkai Hao
- Novogene Bioinformatics Institute, Beijing, China
| | - Aizhen Wang
- College of Eco-Environmental Engineering, Qinghai University, Xi'ning, Qinghai, China
| | - Kirill Sharshov
- Research Institute of Experimental and Clinical Medicine, Novosibirsk, Russia
| | - Alexey Druzyaka
- Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia
| | - Zhuoma Lancuo
- School of Finance and Economics, Qinghai University, Xi'ning, Qinghai, China
| | - Yuetong Shi
- KunLun College of Qinghai University, Xi'ning, Qinghai, China
| | - Shuo Feng
- State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xi'ning, Qinghai, China
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Morris KM, Hindle MM, Boitard S, Burt DW, Danner AF, Eory L, Forrest HL, Gourichon D, Gros J, Hillier LW, Jaffredo T, Khoury H, Lansford R, Leterrier C, Loudon A, Mason AS, Meddle SL, Minvielle F, Minx P, Pitel F, Seiler JP, Shimmura T, Tomlinson C, Vignal A, Webster RG, Yoshimura T, Warren WC, Smith J. The quail genome: insights into social behaviour, seasonal biology and infectious disease response. BMC Biol 2020; 18:14. [PMID: 32050986 PMCID: PMC7017630 DOI: 10.1186/s12915-020-0743-4] [Citation(s) in RCA: 36] [Impact Index Per Article: 7.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/07/2019] [Accepted: 01/24/2020] [Indexed: 12/13/2022] Open
Abstract
BACKGROUND The Japanese quail (Coturnix japonica) is a popular domestic poultry species and an increasingly significant model species in avian developmental, behavioural and disease research. RESULTS We have produced a high-quality quail genome sequence, spanning 0.93 Gb assigned to 33 chromosomes. In terms of contiguity, assembly statistics, gene content and chromosomal organisation, the quail genome shows high similarity to the chicken genome. We demonstrate the utility of this genome through three diverse applications. First, we identify selection signatures and candidate genes associated with social behaviour in the quail genome, an important agricultural and domestication trait. Second, we investigate the effects and interaction of photoperiod and temperature on the transcriptome of the quail medial basal hypothalamus, revealing key mechanisms of photoperiodism. Finally, we investigate the response of quail to H5N1 influenza infection. In quail lung, many critical immune genes and pathways were downregulated after H5N1 infection, and this may be key to the susceptibility of quail to H5N1. CONCLUSIONS We have produced a high-quality genome of the quail which will facilitate further studies into diverse research questions using the quail as a model avian species.
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Affiliation(s)
- Katrina M Morris
- The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK.
| | - Matthew M Hindle
- The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK
| | - Simon Boitard
- GenPhySE, Université de Toulouse, INRAE, ENVT, 31326, Castanet Tolosan, France
| | - David W Burt
- The John Hay Building, Queensland Biosciences Precinct, 306 Carmody Road, The University of Queensland, QLD, St Lucia, 4072, Australia
| | - Angela F Danner
- Virology Division, Department of Infectious Diseases, St. Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN, 38105, USA
| | - Lel Eory
- The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK
| | - Heather L Forrest
- Virology Division, Department of Infectious Diseases, St. Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN, 38105, USA
| | - David Gourichon
- PEAT Pôle d'Expérimentation Avicole de Tours, Centre de recherche Val de Loire, INRAE, 1295, Nouzilly, UE, France
| | - Jerome Gros
- Department of Developmental and Stem Cell Biology, Institut Pasteur, 25 rue du Docteur Roux, 75724, Cedex 15, Paris, France
- CNRS URA3738, 25 rue du Dr Roux, 75015, Paris, France
| | - LaDeana W Hillier
- McDonnell Genome Institute, Washington University School of Medicine, 4444 Forest Park Blvd, St Louis, MO, 63108, USA
| | - Thierry Jaffredo
- CNRS UMR7622, Inserm U 1156, Laboratoire de Biologie du Développement, Sorbonne Université, IBPS, 75005, Paris, France
| | - Hanane Khoury
- CNRS UMR7622, Inserm U 1156, Laboratoire de Biologie du Développement, Sorbonne Université, IBPS, 75005, Paris, France
| | - Rusty Lansford
- Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles and Keck School of Medicine of the University of Southern California, Los Angeles, CA, 90027, USA
| | - Christine Leterrier
- UMR85 Physiologie de la Reproduction et des Comportements, INRAE, CNRS, Université François Rabelais, IFCE, INRAE, Val de Loire, 37380, Nouzilly, Centre, France
| | - Andrew Loudon
- Centre for Biological Timing, Faculty of Biology, Medicine and Health, School of Medical Sciences, University of Manchester, 3.001, A.V. Hill Building, Oxford Road, Manchester, M13 9PT, UK
| | - Andrew S Mason
- The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK
| | - Simone L Meddle
- The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK
| | - Francis Minvielle
- GABI, INRAE, AgroParisTech, Université Paris-Saclay, 78350, Jouy-en-Josas, France
| | - Patrick Minx
- McDonnell Genome Institute, Washington University School of Medicine, 4444 Forest Park Blvd, St Louis, MO, 63108, USA
| | - Frédérique Pitel
- GenPhySE, Université de Toulouse, INRAE, ENVT, 31326, Castanet Tolosan, France
| | - J Patrick Seiler
- Virology Division, Department of Infectious Diseases, St. Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN, 38105, USA
| | - Tsuyoshi Shimmura
- Department of Biological Production, Tokyo University of Agriculture and Technology, 3-8-1 Harumi-cho, Fuchu, Tokyo, 183-8538, Japan
| | - Chad Tomlinson
- McDonnell Genome Institute, Washington University School of Medicine, 4444 Forest Park Blvd, St Louis, MO, 63108, USA
| | - Alain Vignal
- GenPhySE, Université de Toulouse, INRAE, ENVT, 31326, Castanet Tolosan, France
| | - Robert G Webster
- Virology Division, Department of Infectious Diseases, St. Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN, 38105, USA
| | - Takashi Yoshimura
- Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8601, Japan
| | - Wesley C Warren
- Department of Animal Sciences, Department of Surgery, Institute for Data Science and Informatics, University of Missouri, Bond Life Sciences Center, 1201 Rollins Street, Columbia, MO, 65211, USA
| | - Jacqueline Smith
- The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK
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Anatomical Uniqueness of the Mucosal Immune System (GALT, NALT, iBALT) for the Induction and Regulation of Mucosal Immunity and Tolerance. MUCOSAL VACCINES 2020. [PMCID: PMC7149644 DOI: 10.1016/b978-0-12-811924-2.00002-x] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Indexed: 01/16/2023]
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Dhar R, Seethy A, Pethusamy K, Singh S, Rohil V, Purkayastha K, Mukherjee I, Goswami S, Singh R, Raj A, Srivastava T, Acharya S, Rajashekhar B, Karmakar S. De novo assembly of the Indian blue peacock (Pavo cristatus) genome using Oxford Nanopore technology and Illumina sequencing. Gigascience 2019; 8:5488106. [PMID: 31077316 PMCID: PMC6511069 DOI: 10.1093/gigascience/giz038] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/29/2018] [Revised: 09/30/2018] [Accepted: 03/18/2019] [Indexed: 01/23/2023] Open
Abstract
Background The Indian peafowl (Pavo cristanus) is native to South Asia and is the national bird of India. Here we present a draft genome sequence of the male blue peacock using Illumina and Oxford Nanopore technology (ONT). Results ONT sequencing gave ∼2.3-fold sequencing coverage, whereas Illumina generated 150–base pair paired-end sequence data at 284.6-fold coverage from 5 libraries. Subsequently, we generated a 0.915-gigabase pair de novo assembly of the peacock genome with a scaffold N50 of 0.23 megabase pairs (Mb). We predict that the peacock genome contains 23,153 protein-coding genes and 75.3 Mb (7.33%) of repetitive sequences. Conclusions We report a high-quality assembly of the peacock genome using a hybrid approach of sequences generated by both Illumina and ONT. The long-read chemistry generated by ONT was useful for addressing challenges related to de novo assembly, particularly at regions containing repetitive sequences spanning longer than the read length, and which could not be resolved with only short-read–based assembly. Contig assembly of Illumina short reads gave an N50 of 1,639 bases, whereas with ONT, the N50 increased by >9-fold to 14,749 bases. The initial contig assembly based on Illumina sequencing reads alone gave 685,241 contigs. Further scaffolding on assembled contigs using both Illumina and ONT sequencing reads resulted in a final assembly of 15,025 super-scaffolds, with an N50 of ∼0.23 Mb. Ninety-five percent of proteins predicted by homology matched with those in a public repository, verifying the completeness of our assembly. Like other phylogenetic studies of avian conserved genes, we found P. cristatus to be most closely related to Gallus gallus, followed by Meleagris gallopavo and Anas platyrhynchos. Compared with the recently published peacock genome assembly, the current, superior, hybrid assembly has greater sequencing depth, fewer non-ATGC sequences, and fewer scaffolds.
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Affiliation(s)
- Ruby Dhar
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Ashikh Seethy
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Karthikeyan Pethusamy
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Sunil Singh
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Vishwajeet Rohil
- Vallabhbhai Patel Chest Institute (VPCI), Delhi University, New Delhi 110007, India
| | - Kakali Purkayastha
- Vallabhbhai Patel Chest Institute (VPCI), Delhi University, New Delhi 110007, India
| | - Indrani Mukherjee
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Sandeep Goswami
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Rakesh Singh
- Kanpur Zoo, Hastings Ave, Azad Nagar, Nawabganj, Kanpur, Uttar Pradesh 208002, India
| | - Ankita Raj
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Tryambak Srivastava
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Sovon Acharya
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
| | - Balaji Rajashekhar
- Institute of Computer Science, University of Tartu, J. Liivi, Tartu 50409, Estonia.,Celixa, 19/1 Sankey Road, Bangalore 560020, India
| | - Subhradip Karmakar
- Department of Biochemistry, Room 3020, AIIMS - All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
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Zhou C, Yu H, Geng Y, Liu W, Zheng S, Yang N, Meng Y, Dou L, Price M, Ran J, Yue B, Wu Y. A High-Quality Draft Genome Assembly of the Black-Necked Crane (Grus nigricollis) Based on Nanopore Sequencing. Genome Biol Evol 2019; 11:3332-3340. [PMID: 31725151 PMCID: PMC7145580 DOI: 10.1093/gbe/evz251] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 11/13/2019] [Indexed: 11/14/2022] Open
Abstract
The black-necked crane (Grus nigricollis) which inhabits high-altitude areas has the largest body size of the world's 15 crane species, and is classified as threatened by the IUCN. To support further studies on population genetics and genomics, we present a high-quality genome assembly based on both Illumina and nanopore sequencing. In total, 54.59 Gb Illumina short reads and 116.5 Gb nanopore long reads were generated. The 1.23 Gb assembled genome has a high contig N50 of 17.89 Mb, and has a longest contig of 87.83 Mb. The completeness (97.7%) of the draft genome was evaluated with single-copy orthologous genes using BUSCO. We identified 17,789 genes and found that 8.11% of the genome is composed of repetitive elements. In total, 84 of the 2,272 one-to-one orthologous genes were under positive selection in the black-necked crane lineage. SNP-based inference indicated two bottlenecks in the recent demographic trajectories of the black-necked crane. The genome information will contribute to future study of crane evolutionary history and provide new insights into the potential adaptation mechanisms of the black-necked crane to its high-altitude habitat.
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Affiliation(s)
- Chuang Zhou
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Haoran Yu
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Yang Geng
- Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Wei Liu
- College of Life Sciences, Huaibei Normal University, PR China
| | - Shuai Zheng
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Nan Yang
- Institute of Qinghai-Tibetan Plateau, Southwest Minzu University, Chengdu, PR China
| | - Yang Meng
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Liang Dou
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Megan Price
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Jianghong Ran
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Bisong Yue
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
| | - Yongjie Wu
- Key Laboratory of Bioresources and Ecoenvironment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, PR China
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