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Yin J, Li X, Dong L, Zhu X, Chen Y, Zhao W, Liu Y, Shan J, Liu W, Lin C, Miao W. Transformation-based gene silencing and functional characterization of an ISC effector reveal how a powdery mildew fungus disturbs salicylic acid biosynthesis and immune response in the plant. MOLECULAR PLANT PATHOLOGY 2024; 25:e70030. [PMID: 39558488 PMCID: PMC11573735 DOI: 10.1111/mpp.70030] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/24/2024] [Revised: 10/21/2024] [Accepted: 10/31/2024] [Indexed: 11/20/2024]
Abstract
Obligate biotrophic powdery mildew fungi infect a wide range of economically important plants. These fungi often deliver effector proteins into the host tissues to suppress plant immunity and sustain infection. The phytohormone salicylic acid (SA) is one of the most important signals that activate plant immunity against pathogens. However, how powdery mildew effectors interact with host SA signalling is poorly understood. Isochorismatase (ISC) effectors from two other filamentous pathogens have been found to inhibit host SA biosynthesis by hydrolysing isochorismate, the main SA precursor in the plant cytosol. Here, we identified an ISC effector, named EqIsc1, from the rubber tree powdery mildew fungus Erysiphe quercicola. In ISC enzyme assays, EqIsc1 displayed ISC activity by transferring isochorismate to 2,3-dihydro-2,3-dihydroxybenzoate in vitro and in transgenic Nicotiana benthamiana plants. In EqIsc1-expressing transgenic Arabidopsis thaliana, SA biosynthesis and SA-mediated immune response were significantly inhibited. In addition, we developed an electroporation-mediated transformation method for the genetic manipulation of E. quercicola. Inoculation of rubber tree leaves with EqIsc1-silenced E. quercicola strain induced SA-mediated immunity. We also detected the translocation of EqIsc1 into the plant cytosol during the interaction between E. quercicola and its host. Taken together, our results suggest that a powdery mildew effector functions as an ISC enzyme to hydrolyse isochorismate in the host cytosol, altering the SA biosynthesis and immune response.
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Affiliation(s)
- Jinyao Yin
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Xiao Li
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Linpeng Dong
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Xuehuan Zhu
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Yalong Chen
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Wenyuan Zhao
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Yuhan Liu
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Jiaxin Shan
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Wenbo Liu
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Chunhua Lin
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
| | - Weiguo Miao
- Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China
- Danzhou Invasive Species Observation and Research Station of Hainan Province, Hainan University, Danzhou, China
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Lu Y, Yang S, Chen W, Xie H, Xu C. Advances in Migratory Plant Endoparasitic Nematode Effectors. Int J Mol Sci 2024; 25:6435. [PMID: 38928141 PMCID: PMC11203926 DOI: 10.3390/ijms25126435] [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: 04/28/2024] [Revised: 06/01/2024] [Accepted: 06/08/2024] [Indexed: 06/28/2024] Open
Abstract
Unlike sedentary plant-parasitic nematodes, migratory plant endoparasitic nematodes (MPENs) are unable to establish permanent feeding sites, and all developmental stages (except eggs) can invade and feed on plant tissues and can be easily overlooked because of the unspecific symptoms. They cause numerous economic losses in agriculture, forestry, and horticulture. In order to understand the pathogenetic mechanism of MPENs, here we describe research on functions and host targets focused on currently identified effectors from six MPENs, namely Radopholus similis, Pratylenchus spp., Ditylenchus destructor, Bursaphelenchus xylophilus, Aphelenchoides besseyi, and Hirschmanniella oryzae. This information will provide valuable insights into understanding MPEN effectors and for future fostering advancements in plant protection.
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Affiliation(s)
| | | | | | | | - Chunling Xu
- Research Center of Nematodes of Plant Quarantine, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Department of Plant Pathology, College of Plant Protection, South China Agricultural University, Guangzhou 510642, China
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Hu LJ, Wu XQ, Ding XL, Ye JR. Comparative transcriptomic analysis of candidate effectors to explore the infection and survival strategy of Bursaphelenchus xylophilus during different interaction stages with pine trees. BMC PLANT BIOLOGY 2021; 21:224. [PMID: 34011295 PMCID: PMC8132355 DOI: 10.1186/s12870-021-02993-9] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/21/2020] [Accepted: 04/27/2021] [Indexed: 05/02/2023]
Abstract
BACKGROUND The pine wood nematode (PWN), Bursaphelenchus xylophilus, is a devastating pathogen of many Pinus species in China. The aim of this study was to understand the interactive molecular mechanism of PWN and its host by comparing differentially expressed genes and candidate effectors from three transcriptomes of B. xylophilus at different infection stages. RESULTS In total, 62, 69 and 46 candidate effectors were identified in three transcriptomes (2.5 h postinfection, 6, 12 and 24 h postinoculation and 6 and 15 d postinfection, respectively). In addition to uncharacterized pioneers, other candidate effectors were involved in the degradation of host tissues, suppression of host defenses, targeting plant signaling pathways, feeding and detoxification, which helped B. xylophilus survive successfully in the host. Seven candidate effectors were identified in both our study and the B. xylophilus transcriptome at 2.5 h postinfection, and one candidate effector was identified in all three transcriptomes. These common candidate effectors were upregulated at infection stages, and one of them suppressed pathogen-associated molecular pattern (PAMP) PsXEG1-triggered cell death in Nicotiana benthamiana. CONCLUSIONS The results indicated that B. xylophilus secreted various candidate effectors, and some of them continued to function throughout all infection stages. These various candidate effectors were important to B. xylophilus infection and survival, and they functioned in different ways (such as breaking down host cell walls, suppressing host defenses, promoting feeding efficiency, promoting detoxification and playing virulence functions). The present results provide valuable resources for in-depth research on the pathogenesis of B. xylophilus from the perspective of effectors.
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Affiliation(s)
- Long-Jiao Hu
- Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China
- Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University, Nanjing, 210037, China
| | - Xiao-Qin Wu
- Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China.
- Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University, Nanjing, 210037, China.
| | - Xiao-Lei Ding
- Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China
- Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University, Nanjing, 210037, China
| | - Jian-Ren Ye
- Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China
- Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University, Nanjing, 210037, China
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Bauters L, Kyndt T, De Meyer T, Morreel K, Boerjan W, Lefevere H, Gheysen G. Chorismate mutase and isochorismatase, two potential effectors of the migratory nematode Hirschmanniella oryzae, increase host susceptibility by manipulating secondary metabolite content of rice. MOLECULAR PLANT PATHOLOGY 2020; 21:1634-1646. [PMID: 33084136 PMCID: PMC7694671 DOI: 10.1111/mpp.13003] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/28/2020] [Revised: 09/07/2020] [Accepted: 09/07/2020] [Indexed: 05/11/2023]
Abstract
Hirschmanniella oryzae is one of the most devastating nematodes on rice, leading to substantial yield losses. Effector proteins aid the nematode during the infection process by subduing plant defence responses. In this research we characterized two potential H. oryzae effector proteins, chorismate mutase (HoCM) and isochorismatase (HoICM), and investigated their enzymatic activity and their role in plant immunity. Both HoCM and HoICM proved to be enzymatically active in complementation tests in mutant Escherichia coli strains. Infection success by the migratory nematode H. oryzae was significantly higher in transgenic rice lines constitutively expressing HoCM or HoICM. Expression of HoCM, but not HoICM, increased rice susceptibility against the sedentary nematode Meloidogyne graminicola also. Transcriptome and metabolome analyses indicated reductions in secondary metabolites in the transgenic rice plants expressing the potential nematode effectors. The results presented here demonstrate that both HoCM and HoICM suppress the host immune system and that this may be accomplished by lowering secondary metabolite levels in the plant.
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Affiliation(s)
- Lander Bauters
- Department of BiotechnologyFaculty of Bioscience EngineeringGhent UniversityGhentBelgium
| | - Tina Kyndt
- Department of BiotechnologyFaculty of Bioscience EngineeringGhent UniversityGhentBelgium
| | - Tim De Meyer
- Department of Data Analysis and Mathematical ModellingFaculty of Bioscience EngineeringGhent UniversityGhentBelgium
| | - Kris Morreel
- VIB‐UGent Center for Plant Systems BiologyGhentBelgium
- Department of Plant Biotechnology and BioinformaticsFaculty of SciencesGhent UniversityGhentBelgium
| | - Wout Boerjan
- VIB‐UGent Center for Plant Systems BiologyGhentBelgium
- Department of Plant Biotechnology and BioinformaticsFaculty of SciencesGhent UniversityGhentBelgium
| | - Hannes Lefevere
- Department of BiotechnologyFaculty of Bioscience EngineeringGhent UniversityGhentBelgium
| | - Godelieve Gheysen
- Department of BiotechnologyFaculty of Bioscience EngineeringGhent UniversityGhentBelgium
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5
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Lefevere H, Bauters L, Gheysen G. Salicylic Acid Biosynthesis in Plants. FRONTIERS IN PLANT SCIENCE 2020; 11:338. [PMID: 32362901 PMCID: PMC7182001 DOI: 10.3389/fpls.2020.00338] [Citation(s) in RCA: 248] [Impact Index Per Article: 49.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 12/20/2019] [Accepted: 03/06/2020] [Indexed: 05/19/2023]
Abstract
Salicylic acid (SA) is an important plant hormone that is best known for mediating host responses upon pathogen infection. Its role in plant defense activation is well established, but its biosynthesis in plants is not fully understood. SA is considered to be derived from two possible pathways; the ICS and PAL pathway, both starting from chorismate. The importance of both pathways for biosynthesis differs between plant species, rendering it hard to make generalizations about SA production that cover the entire plant kingdom. Yet, understanding SA biosynthesis is important to gain insight into how plant pathogen responses function and how pathogens can interfere with them. In this review, we have taken a closer look at how SA is synthesized and the importance of both biosynthesis pathways in different plant species.
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Affiliation(s)
| | | | - Godelieve Gheysen
- Department of Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
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6
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RNA-Seq revealed that infection with white tip nematodes could downregulate rice photosynthetic genes. Funct Integr Genomics 2019; 20:367-381. [DOI: 10.1007/s10142-019-00717-9] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/16/2019] [Revised: 07/21/2019] [Accepted: 09/20/2019] [Indexed: 10/25/2022]
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Hu LJ, Wu XQ, Li HY, Zhao Q, Wang YC, Ye JR. An Effector, BxSapB1, Induces Cell Death and Contributes to Virulence in the Pine Wood Nematode Bursaphelenchus xylophilus. MOLECULAR PLANT-MICROBE INTERACTIONS : MPMI 2019; 32:452-463. [PMID: 30351223 DOI: 10.1094/mpmi-10-18-0275-r] [Citation(s) in RCA: 12] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/18/2023]
Abstract
The pine wood nematode (PWN) Bursaphelenchus xylophilus has caused serious damage to pine forests in China. Effectors secreted by phytonematodes play a role in host infection. We identified and characterized an effector, BxSapB1, based on the B. xylophilus transcriptome at the early stages of infection and the transient expression of proteins in Nicotiana benthamiana. BxSapB1 triggered cell death in N. benthamiana when secreted into the apoplast, and this effect was independent of N. benthamiana brassinosteroid-insensitive 1-associated kinase 1 (NbBAK1) and suppressor of BIR1-1 (NbSOBIR1). The signal peptide of BxSapB1 was proven to be functional in yeast using the yeast signal sequence trap system and BxSapB1 was strongly expressed in the subventral gland cells of B. xylophilus, as revealed by in-situ hybridization. In addition, based on local BLAST analysis, the BxSapB1 showed 100% identity to BUX.s00139.62, which was identified from the B. xylophilus secretome during Pinus thunbergii infection. BxSapB1 was upregulated in a highly virulent strain and downregulated in a weakly virulent strain of PWN at the early stages of infection. RNA interference assays showed that silencing BxSapB1 resulted in decreased expression of pathogenesis-related genes (PtPR-1b, PtPR-3, and PtPR-5) as well as delayed onset of symptoms in P. thunbergii infected by B. xylophilus. The combined data suggest that BxSapB1 can trigger cell death in N. benthamiana and that it contributes to the virulence in B. xylophilus during parasitic interaction.
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Affiliation(s)
- Long-Jiao Hu
- 1 Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China
- 2 Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University; and
| | - Xiao-Qin Wu
- 1 Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China
- 2 Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University; and
| | - Hai-Yang Li
- 3 Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China
| | - Qun Zhao
- 1 Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China
- 2 Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University; and
| | - Yuan-Chao Wang
- 3 Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China
| | - Jian-Ren Ye
- 1 Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China
- 2 Jiangsu Key Laboratory for Prevention and Management of Invasive Species, Nanjing Forestry University; and
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8
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Gheysen G, Mitchum MG. Phytoparasitic Nematode Control of Plant Hormone Pathways. PLANT PHYSIOLOGY 2019; 179:1212-1226. [PMID: 30397024 PMCID: PMC6446774 DOI: 10.1104/pp.18.01067] [Citation(s) in RCA: 69] [Impact Index Per Article: 11.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/28/2018] [Accepted: 10/24/2018] [Indexed: 05/17/2023]
Abstract
Phytoparasitic nematodes use multiple tactics to influence phytohormone physiology and alter plant developmental programs to establish feeding sites.
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Affiliation(s)
- Godelieve Gheysen
- Ghent University, Department of Biotechnology, Coupure Links 653, 9000 Ghent, Belgium
| | - Melissa G Mitchum
- University of Missouri, Division of Plant Sciences and Bond Life Sciences Center, Columbia, Missouri 65211
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9
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Rancurel C, Legrand L, Danchin EGJ. Alienness: Rapid Detection of Candidate Horizontal Gene Transfers across the Tree of Life. Genes (Basel) 2017; 8:E248. [PMID: 28961181 PMCID: PMC5664098 DOI: 10.3390/genes8100248] [Citation(s) in RCA: 31] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/31/2017] [Revised: 09/22/2017] [Accepted: 09/22/2017] [Indexed: 11/22/2022] Open
Abstract
Horizontal gene transfer (HGT) is the transmission of genes between organisms by other means than parental to offspring inheritance. While it is prevalent in prokaryotes, HGT is less frequent in eukaryotes and particularly in Metazoa. Here, we propose Alienness, a taxonomy-aware web application available at http://alienness.sophia.inra.fr. Alienness parses BLAST results against public libraries to rapidly identify candidate HGT in any genome of interest. Alienness takes as input the result of a BLAST of a whole proteome of interest against any National Center for Biotechnology Information (NCBI) protein library. The user defines recipient (e.g., Metazoa) and donor (e.g., bacteria, fungi) branches of interest in the NCBI taxonomy. Based on the best BLAST E-values of candidate donor and recipient taxa, Alienness calculates an Alien Index (AI) for each query protein. An AI > 0 indicates a better hit to candidate donor than recipient taxa and a possible HGT. Higher AI represent higher gap of E-values between candidate donor and recipient and a more likely HGT. We confirmed the accuracy of Alienness on phylogenetically confirmed HGT of non-metazoan origin in plant-parasitic nematodes. Alienness scans whole proteomes to rapidly identify possible HGT in any species of interest and thus fosters exploration of HGT more easily and largely across the tree of life.
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Affiliation(s)
- Corinne Rancurel
- INRA, CNRS, ISA, Université Côte d'Azur, 06903 Sophia Antipolis Cedex, France.
| | - Ludovic Legrand
- LIPM, INRA, CNRS, Université de Toulouse, 31326 Castanet-Tolosan Cedex, France.
| | - Etienne G J Danchin
- INRA, CNRS, ISA, Université Côte d'Azur, 06903 Sophia Antipolis Cedex, France.
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Kikuchi T, Eves-van den Akker S, Jones JT. Genome Evolution of Plant-Parasitic Nematodes. ANNUAL REVIEW OF PHYTOPATHOLOGY 2017; 55:333-354. [PMID: 28590877 DOI: 10.1146/annurev-phyto-080516-035434] [Citation(s) in RCA: 50] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/12/2023]
Abstract
Plant parasitism has evolved independently on at least four separate occasions in the phylum Nematoda. The application of next-generation sequencing (NGS) to plant-parasitic nematodes has allowed a wide range of genome- or transcriptome-level comparisons, and these have identified genome adaptations that enable parasitism of plants. Current genome data suggest that horizontal gene transfer, gene family expansions, evolution of new genes that mediate interactions with the host, and parasitism-specific gene regulation are important adaptations that allow nematodes to parasitize plants. Sequencing of a larger number of nematode genomes, including plant parasites that show different modes of parasitism or that have evolved in currently unsampled clades, and using free-living taxa as comparators would allow more detailed analysis and a better understanding of the organization of key genes within the genomes. This would facilitate a more complete understanding of the way in which parasitism has shaped the genomes of plant-parasitic nematodes.
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Affiliation(s)
- Taisei Kikuchi
- Division of Parasitology, Faculty of Medicine, University of Miyazaki, Miyazaki 889-1692, Japan;
| | - Sebastian Eves-van den Akker
- Division of Plant Sciences, College of Life Sciences, University of Dundee, Dundee, DD1 5EH, United Kingdom
- Department of Biological Chemistry, The John Innes Centre, Norwich, NR4 7UH, United Kingdom
| | - John T Jones
- Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Invergowrie, Dundee, DD2 5DA, United Kingdom
- School of Biology, University of St. Andrews, North Haugh, St. Andrews, KY16 9TZ, United Kingdom
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11
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The Distribution of Lectins across the Phylum Nematoda: A Genome-Wide Search. Int J Mol Sci 2017; 18:ijms18010091. [PMID: 28054982 PMCID: PMC5297725 DOI: 10.3390/ijms18010091] [Citation(s) in RCA: 21] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/18/2016] [Revised: 12/20/2016] [Accepted: 12/28/2016] [Indexed: 12/13/2022] Open
Abstract
Nematodes are a very diverse phylum that has adapted to nearly every ecosystem. They have developed specialized lifestyles, dividing the phylum into free-living, animal, and plant parasitic species. Their sheer abundance in numbers and presence in nearly every ecosystem make them the most prevalent animals on earth. In this research nematode-specific profiles were designed to retrieve predicted lectin-like domains from the sequence data of nematode genomes and transcriptomes. Lectins are carbohydrate-binding proteins that play numerous roles inside and outside the cell depending on their sugar specificity and associated protein domains. The sugar-binding properties of the retrieved lectin-like proteins were predicted in silico. Although most research has focused on C-type lectin-like, galectin-like, and calreticulin-like proteins in nematodes, we show that the lectin-like repertoire in nematodes is far more diverse. We focused on C-type lectins, which are abundantly present in all investigated nematode species, but seem to be far more abundant in free-living species. Although C-type lectin-like proteins are omnipresent in nematodes, we have shown that only a small part possesses the residues that are thought to be essential for carbohydrate binding. Curiously, hevein, a typical plant lectin domain not reported in animals before, was found in some nematode species.
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12
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Kaliyappan R, Viswanathan S, Suthanthiram B, Subbaraya U, Marimuthu Somasundram S, Muthu M. Evolutionary Expansion of WRKY Gene Family in Banana and Its Expression Profile during the Infection of Root Lesion Nematode, Pratylenchus coffeae. PLoS One 2016; 11:e0162013. [PMID: 27603787 PMCID: PMC5014340 DOI: 10.1371/journal.pone.0162013] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/19/2015] [Accepted: 08/16/2016] [Indexed: 11/18/2022] Open
Abstract
The WRKY family of transcription factors orchestrate the reprogrammed expression of the complex network of defense genes at various biotic and abiotic stresses. Within the last 96 million years, three rounds of Musa polyploidization events had occurred from selective pressure causing duplication of MusaWRKYs with new activities. Here, we identified a total of 153 WRKY transcription factors available from the DH Pahang genome. Based on their phylogenetic relationship, the MusaWRKYs available with complete gene sequence were classified into the seven common WRKY sub-groups. Synteny analyses data revealed paralogous relationships, with 17 MusaWRKY gene pairs originating from the duplication events that had occurred within the Musa lineage. We also found 15 other MusaWRKY gene pairs originating from much older duplication events that had occurred along Arecales and Poales lineage of commelinids. Based on the synonymous and nonsynonymous substitution rates, the fate of duplicated MusaWRKY genes was predicted to have undergone sub-functionalization in which the duplicated gene copies retain a subset of the ancestral gene function. Also, to understand the regulatory roles of MusaWRKY during a biotic stress, Illumina sequencing was performed on resistant and susceptible cultivars during the infection of root lesion nematode, Pratylenchus coffeae. The differential WRKY gene expression analysis in nematode resistant and susceptible cultivars during challenged and unchallenged conditions had distinguished: 1) MusaWRKYs participating in general banana defense mechanism against P.coffeae common to both susceptible and resistant cultivars, 2) MusaWRKYs that may aid in the pathogen survival as suppressors of plant triggered immunity, 3) MusaWRKYs that may aid in the host defense as activators of plant triggered immunity and 4) cultivar specific MusaWRKY regulation. Mainly, MusaWRKY52, -69 and -92 are found to be P.coffeae specific and can act as activators or repressors in a defense pathway. Overall, this preliminary study in Musa provides the basis for understanding the evolution and regulatory mechanism of MusaWRKY during nematode stress.
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Affiliation(s)
- Raja Kaliyappan
- Crop Improvement Division, ICAR-National Research Centre for Banana, Tamil Nadu, Tiruchirapalli, India
| | - Sriram Viswanathan
- Crop Improvement Division, ICAR-National Research Centre for Banana, Tamil Nadu, Tiruchirapalli, India
| | - Backiyarani Suthanthiram
- Crop Improvement Division, ICAR-National Research Centre for Banana, Tamil Nadu, Tiruchirapalli, India
- * E-mail:
| | - Uma Subbaraya
- Crop Improvement Division, ICAR-National Research Centre for Banana, Tamil Nadu, Tiruchirapalli, India
| | | | - Mayilvaganan Muthu
- Crop Improvement Division, ICAR-National Research Centre for Banana, Tamil Nadu, Tiruchirapalli, India
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Fosu-Nyarko J, Jones MGK. Advances in Understanding the Molecular Mechanisms of Root Lesion Nematode Host Interactions. ANNUAL REVIEW OF PHYTOPATHOLOGY 2016; 54:253-78. [PMID: 27296144 DOI: 10.1146/annurev-phyto-080615-100257] [Citation(s) in RCA: 37] [Impact Index Per Article: 4.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/20/2023]
Abstract
Root lesion nematodes (RLNs) are one of the most economically important groups of plant nematodes. As migratory endoparasites, their presence in roots is less obvious than infestations of sedentary endoparasites; nevertheless, in many instances, they are the major crop pests. With increasing molecular information on nematode parasitism, available data now reflect the differences and, in particular, similarities in lifestyle between migratory and sedentary endoparasites. Far from being unsophisticated compared with sedentary endoparasites, migratory endoparasites are exquisitely suited to their parasitic lifestyle. What they lack in effectors required for induction of permanent feeding sites, they make up for with their versatile host range and their ability to move and feed from new host roots and survive adverse conditions. In this review, we summarize the current molecular data available for RLNs and highlight differences and similarities in effectors and molecular mechanisms between migratory and sedentary endoparasitic nematodes.
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Affiliation(s)
- John Fosu-Nyarko
- Plant Biotechnology Research Group, School of Veterinary and Life Sciences, Western Australian State Agricultural Biotechnology Centre, Murdoch University, Perth, Western Australia 6150, Australia; ,
| | - Michael G K Jones
- Plant Biotechnology Research Group, School of Veterinary and Life Sciences, Western Australian State Agricultural Biotechnology Centre, Murdoch University, Perth, Western Australia 6150, Australia; ,
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14
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Petitot AS, Dereeper A, Agbessi M, Da Silva C, Guy J, Ardisson M, Fernandez D. Dual RNA-seq reveals Meloidogyne graminicola transcriptome and candidate effectors during the interaction with rice plants. MOLECULAR PLANT PATHOLOGY 2016; 17:860-74. [PMID: 26610268 PMCID: PMC6638361 DOI: 10.1111/mpp.12334] [Citation(s) in RCA: 43] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/16/2015] [Revised: 10/09/2015] [Accepted: 10/09/2015] [Indexed: 05/15/2023]
Abstract
Root-knot nematodes secrete proteinaceous effectors into plant tissues to facilitate infection by suppressing host defences and reprogramming the host metabolism to their benefit. Meloidogyne graminicola is a major pest of rice (Oryza sativa) in Asia and Latin America, causing important crop losses. The goal of this study was to identify M. graminicola pathogenicity genes expressed during the plant-nematode interaction. Using the dual RNA-sequencing (RNA-seq) strategy, we generated transcriptomic data of M. graminicola samples covering the pre-parasitic J2 stage and five parasitic stages in rice plants, from the parasitic J2 to the adult female. In the absence of a reference genome, a de novo M. graminicola transcriptome of 66 396 contigs was obtained from those reads that were not mapped on the rice genome. Gene expression profiling across the M. graminicola life cycle revealed key genes involved in nematode development and provided insights into the genes putatively associated with parasitism. The development of a 'secreted protein prediction' pipeline revealed a typical set of proteins secreted by nematodes, as well as a large number of cysteine-rich proteins and putative nuclear proteins. Combined with expression data, this pipeline enabled the identification of 15 putative effector genes, including two homologues of well-characterized effectors from cyst nematodes (CLE-like and VAP1) and a metallothionein. The localization of gene expression was assessed by in situ hybridization for a subset of candidates. All of these data represent important molecular resources for the elucidation of M. graminicola biology and for the selection of potential targets for the development of novel control strategies for this nematode species.
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Affiliation(s)
- Anne-Sophie Petitot
- IRD, UMR IRD-Cirad-UM2 Interactions Plantes-Microbes-Environnement, 34394, Montpellier Cedex 5, France
| | - Alexis Dereeper
- IRD, UMR IRD-Cirad-UM2 Interactions Plantes-Microbes-Environnement, 34394, Montpellier Cedex 5, France
| | - Mawusse Agbessi
- IRD, UMR IRD-Cirad-UM2 Interactions Plantes-Microbes-Environnement, 34394, Montpellier Cedex 5, France
| | - Corinne Da Silva
- CEA, Institut de Génomique, GENOSCOPE - Centre National de Séquençage, 91057, Evry Cedex, France
| | - Julie Guy
- CEA, Institut de Génomique, GENOSCOPE - Centre National de Séquençage, 91057, Evry Cedex, France
| | - Morgane Ardisson
- INRA, UMR Amélioration Génétique et Adaptation des Plantes, 34060, Montpellier Cedex 1, France
| | - Diana Fernandez
- IRD, UMR IRD-Cirad-UM2 Interactions Plantes-Microbes-Environnement, 34394, Montpellier Cedex 5, France
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15
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Eves-van den Akker S, Laetsch DR, Thorpe P, Lilley CJ, Danchin EGJ, Da Rocha M, Rancurel C, Holroyd NE, Cotton JA, Szitenberg A, Grenier E, Montarry J, Mimee B, Duceppe MO, Boyes I, Marvin JMC, Jones LM, Yusup HB, Lafond-Lapalme J, Esquibet M, Sabeh M, Rott M, Overmars H, Finkers-Tomczak A, Smant G, Koutsovoulos G, Blok V, Mantelin S, Cock PJA, Phillips W, Henrissat B, Urwin PE, Blaxter M, Jones JT. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. Genome Biol 2016; 17:124. [PMID: 27286965 PMCID: PMC4901422 DOI: 10.1186/s13059-016-0985-1] [Citation(s) in RCA: 109] [Impact Index Per Article: 12.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/08/2016] [Accepted: 05/12/2016] [Indexed: 11/23/2022] Open
Abstract
Background The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes. Results We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative ‘effector islands’ in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking. Conclusions These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action. Electronic supplementary material The online version of this article (doi:10.1186/s13059-016-0985-1) contains supplementary material, which is available to authorized users.
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Affiliation(s)
| | - Dominik R Laetsch
- Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3FL, UK
| | - Peter Thorpe
- Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK
| | | | - Etienne G J Danchin
- INRA, University Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France
| | - Martine Da Rocha
- INRA, University Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France
| | - Corinne Rancurel
- INRA, University Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France
| | - Nancy E Holroyd
- Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, CB10 1SA, UK
| | - James A Cotton
- Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, CB10 1SA, UK
| | - Amir Szitenberg
- School of Biological, Biomedical and Environmental Sciences, University of Hull, Hull, HU6 7RX, UK
| | - Eric Grenier
- INRA, UMR1349 IGEPP (Institute for Genetics, Environment and Plant Protection), 35653, Le Rheu, France
| | - Josselin Montarry
- INRA, UMR1349 IGEPP (Institute for Genetics, Environment and Plant Protection), 35653, Le Rheu, France
| | - Benjamin Mimee
- Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada
| | - Marc-Olivier Duceppe
- Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada
| | - Ian Boyes
- Sidney Laboratory, Canadian Food Inspection Agency (CFIA), 8801 East Saanich Rd, Sidney, BC, V8L 1H3, Canada
| | | | - Laura M Jones
- Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK
| | - Hazijah B Yusup
- Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK
| | - Joël Lafond-Lapalme
- Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada
| | - Magali Esquibet
- INRA, UMR1349 IGEPP (Institute for Genetics, Environment and Plant Protection), 35653, Le Rheu, France
| | - Michael Sabeh
- Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada
| | - Michael Rott
- Sidney Laboratory, Canadian Food Inspection Agency (CFIA), 8801 East Saanich Rd, Sidney, BC, V8L 1H3, Canada
| | - Hein Overmars
- Laboratory of Nematology, Department of Plant Sciences, Wageningen University, Droevendaalsesteeg 1, 6708, PB, Wageningen, The Netherlands
| | - Anna Finkers-Tomczak
- Laboratory of Nematology, Department of Plant Sciences, Wageningen University, Droevendaalsesteeg 1, 6708, PB, Wageningen, The Netherlands
| | - Geert Smant
- Laboratory of Nematology, Department of Plant Sciences, Wageningen University, Droevendaalsesteeg 1, 6708, PB, Wageningen, The Netherlands
| | | | - Vivian Blok
- Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK
| | - Sophie Mantelin
- Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK
| | - Peter J A Cock
- Information and Computational Sciences Group, James Hutton Institute, Dundee, UK
| | - Wendy Phillips
- USDA-ARS Horticultural Crops Research Laboratory, Corvallis, OR, USA
| | - Bernard Henrissat
- CNRS UMR 7257, INRA, USC 1408, Aix-Marseille University, AFMB, 13288, Marseille, France.,Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia
| | - Peter E Urwin
- Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK
| | - Mark Blaxter
- Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3FL, UK
| | - John T Jones
- Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK.,School of Biology, University of St Andrews, North Haugh, St Andrews, KY16 9TZ, UK
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16
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Noon JB, Baum TJ. Horizontal gene transfer of acetyltransferases, invertases and chorismate mutases from different bacteria to diverse recipients. BMC Evol Biol 2016; 16:74. [PMID: 27068610 PMCID: PMC4828791 DOI: 10.1186/s12862-016-0651-y] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/27/2016] [Accepted: 04/05/2016] [Indexed: 11/24/2022] Open
Abstract
BACKGROUND Hoplolaimina plant-parasitic nematodes (PPN) are a lineage of animals with many documented cases of horizontal gene transfer (HGT). In a recent study, we reported on three likely HGT candidate genes in the soybean cyst nematode Heterodera glycines, all of which encode secreted candidate effectors with putative functions in the host plant. Hg-GLAND1 is a putative GCN5-related N-acetyltransferase (GNAT), Hg-GLAND13 is a putative invertase (INV), and Hg-GLAND16 is a putative chorismate mutase (CM), and blastp searches of the non-redundant database resulted in highest similarity to bacterial sequences. Here, we searched nematode and non-nematode sequence databases to identify all the nematodes possible that contain these three genes, and to formulate hypotheses about when they most likely appeared in the phylum Nematoda. We then performed phylogenetic analyses combined with model selection tests of alternative models of sequence evolution to determine whether these genes were horizontally acquired from bacteria. RESULTS Mining of nematode sequence databases determined that GNATs appeared in Hoplolaimina PPN late in evolution, while both INVs and CMs appeared before the radiation of the Hoplolaimina suborder. Also, Hoplolaimina GNATs, INVs and CMs formed well-supported clusters with different rhizosphere bacteria in the phylogenetic trees, and the model selection tests greatly supported models of HGT over descent via common ancestry. Surprisingly, the phylogenetic trees also revealed additional, well-supported clusters of bacterial GNATs, INVs and CMs with diverse eukaryotes and archaea. There were at least eleven and eight well-supported clusters of GNATs and INVs, respectively, from different bacteria with diverse eukaryotes and archaea. Though less frequent, CMs from different bacteria formed supported clusters with multiple different eukaryotes. Moreover, almost all individual clusters containing bacteria and eukaryotes or archaea contained species that inhabit very similar niches. CONCLUSIONS GNATs were horizontally acquired late in Hoplolaimina PPN evolution from bacteria most similar to the saprophytic and plant-pathogenic actinomycetes. INVs and CMs were horizontally acquired from bacteria most similar to rhizobacteria and Burkholderia soil bacteria, respectively, before the radiation of Hoplolaimina. Also, these three gene groups appear to have been frequent subjects of HGT from different bacteria to numerous, diverse lineages of eukaryotes and archaea, which suggests that these genes may confer important evolutionary advantages to many taxa. In the case of Hoplolaimina PPN, this advantage likely was an improved ability to parasitize plants.
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Affiliation(s)
- Jason B. Noon
- Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA 50011 USA
| | - Thomas J. Baum
- Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA 50011 USA
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17
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Danchin EGJ, Guzeeva EA, Mantelin S, Berepiki A, Jones JT. Horizontal Gene Transfer from Bacteria Has Enabled the Plant-Parasitic Nematode Globodera pallida to Feed on Host-Derived Sucrose. Mol Biol Evol 2016; 33:1571-9. [PMID: 26915958 DOI: 10.1093/molbev/msw041] [Citation(s) in RCA: 39] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/14/2022] Open
Abstract
The evolution of plant-parasitic nematodes (PPN) is unusual in that these organisms have acquired a range of genes from bacteria via horizontal gene transfer (HGT). The proteins encoded by most of these genes are involved in metabolism of various components of the plant cell wall during invasion of the host. Recent genome sequencing projects for PPN have shown that Glycosyl Hydrolase Family 32 (GH32) sequences are present in several PPN species. These sequences are absent from almost all other animals. Here, we show that the GH32 sequences from an economically important cyst nematode species, Globodera pallida are functional invertases, are expressed during feeding and are restricted in expression to the nematode digestive system. These data are consistent with a role in metabolizing host-derived sucrose. In addition, a detailed phylogenetic analysis shows that the GH32 sequences from PPN and those present in some insect species have distinct bacterial origins and do not therefore derive from a gene present in the last common ancestor of ecdysozoan species. HGT has therefore played at least two critical roles in the evolution of PPN, enabling both invasion of the host and feeding on the main translocation carbohydrate of the plant.
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Affiliation(s)
- Etienne G J Danchin
- Institut Sophia Agrobiotech, INRA, Univ. Nice Sophia Antipolis, CNRS, 06903, Sophia Antipolis, France
| | - Elena A Guzeeva
- Dundee Effector Consortium, The James Hutton Institute, Dundee, United Kingdom Centre of Parasitology of the A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia
| | - Sophie Mantelin
- Dundee Effector Consortium, The James Hutton Institute, Dundee, United Kingdom
| | - Adokiye Berepiki
- Dundee Effector Consortium, The James Hutton Institute, Dundee, United Kingdom
| | - John T Jones
- Dundee Effector Consortium, The James Hutton Institute, Dundee, United Kingdom Biology Department, University of St Andrews, St Andrews, Fife, United Kingdom
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18
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Vieira P, Eves-van den Akker S, Verma R, Wantoch S, Eisenback JD, Kamo K. The Pratylenchus penetrans Transcriptome as a Source for the Development of Alternative Control Strategies: Mining for Putative Genes Involved in Parasitism and Evaluation of in planta RNAi. PLoS One 2015; 10:e0144674. [PMID: 26658731 PMCID: PMC4684371 DOI: 10.1371/journal.pone.0144674] [Citation(s) in RCA: 31] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/25/2015] [Accepted: 11/20/2015] [Indexed: 11/25/2022] Open
Abstract
The root lesion nematode Pratylenchus penetrans is considered one of the most economically important species within the genus. Host range studies have shown that nearly 400 plant species can be parasitized by this species. To obtain insight into the transcriptome of this migratory plant-parasitic nematode, we used Illumina mRNA sequencing analysis of a mixed population, as well as nematode reads detected in infected soybean roots 3 and 7 days after nematode infection. Over 140 million paired end reads were obtained for this species, and de novo assembly resulted in a total of 23,715 transcripts. Homology searches showed significant hit matches to 58% of the total number of transcripts using different protein and EST databases. In general, the transcriptome of P. penetrans follows common features reported for other root lesion nematode species. We also explored the efficacy of RNAi, delivered from the host, as a strategy to control P. penetrans, by targeted knock-down of selected nematode genes. Different comparisons were performed to identify putative nematode genes with a role in parasitism, resulting in the identification of transcripts with similarities to other nematode parasitism genes. Focusing on the predicted nematode secreted proteins found in this transcriptome, we observed specific members to be up-regulated at the early time points of infection. In the present study, we observed an enrichment of predicted secreted proteins along the early time points of parasitism by this species, with a significant number being pioneer candidate genes. A representative set of genes examined using RT-PCR confirms their expression during the host infection. The expression patterns of the different candidate genes raise the possibility that they might be involved in critical steps of P. penetrans parasitism. This analysis sheds light on the transcriptional changes that accompany plant infection by P. penetrans, and will aid in identifying potential gene targets for selection and use to design effective control strategies against root lesion nematodes.
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Affiliation(s)
- Paulo Vieira
- Dept. of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, VA, 24061, United States of America
- Floral and Nursery Plants Research Unit, U.S. National Arboretum, U.S. Department of Agriculture, Beltsville, MD, 20705–2350, United States of America
| | | | - Ruchi Verma
- Floral and Nursery Plants Research Unit, U.S. National Arboretum, U.S. Department of Agriculture, Beltsville, MD, 20705–2350, United States of America
| | - Sarah Wantoch
- Floral and Nursery Plants Research Unit, U.S. National Arboretum, U.S. Department of Agriculture, Beltsville, MD, 20705–2350, United States of America
| | - Jonathan D. Eisenback
- Dept. of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, VA, 24061, United States of America
| | - Kathryn Kamo
- Floral and Nursery Plants Research Unit, U.S. National Arboretum, U.S. Department of Agriculture, Beltsville, MD, 20705–2350, United States of America
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19
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Kyndt T, Denil S, Bauters L, Van Criekinge W, De Meyer T. Systemic suppression of the shoot metabolism upon rice root nematode infection. PLoS One 2014; 9:e106858. [PMID: 25216177 PMCID: PMC4162577 DOI: 10.1371/journal.pone.0106858] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/11/2014] [Accepted: 08/10/2014] [Indexed: 11/19/2022] Open
Abstract
Hirschmanniella oryzae is the most common plant-parasitic nematode in flooded rice cultivation systems. These migratory animals penetrate the plant roots and feed on the root cells, creating large cavities, extensive root necrosis and rotting. The objective of this study was to investigate the systemic response of the rice plant upon root infection by this nematode. RNA sequencing was applied on the above-ground parts of the rice plants at 3 and 7 days post inoculation. The data revealed significant modifications in the primary metabolism of the plant shoot, with a general suppression of for instance chlorophyll biosynthesis, the brassinosteroid pathway, and amino acid production. In the secondary metabolism, we detected a repression of the isoprenoid and shikimate pathways. These molecular changes can have dramatic consequences for the growth and yield of the rice plants, and could potentially change their susceptibility to above-ground pathogens and pests.
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Affiliation(s)
- Tina Kyndt
- Department of Molecular Biotechnology, Ghent University, Ghent, Belgium
- * E-mail:
| | - Simon Denil
- Department of Mathematical Modelling, Statistics and Bioinformatics, Ghent University, Ghent, Belgium
| | - Lander Bauters
- Department of Molecular Biotechnology, Ghent University, Ghent, Belgium
| | - Wim Van Criekinge
- Department of Mathematical Modelling, Statistics and Bioinformatics, Ghent University, Ghent, Belgium
- NXTGNT, Ghent University Hospital, Ghent, Belgium
| | - Tim De Meyer
- Department of Mathematical Modelling, Statistics and Bioinformatics, Ghent University, Ghent, Belgium
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20
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Liu T, Song T, Zhang X, Yuan H, Su L, Li W, Xu J, Liu S, Chen L, Chen T, Zhang M, Gu L, Zhang B, Dou D. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun 2014; 5:4686. [PMID: 25156390 PMCID: PMC4348438 DOI: 10.1038/ncomms5686] [Citation(s) in RCA: 233] [Impact Index Per Article: 21.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/02/2014] [Accepted: 07/14/2014] [Indexed: 11/23/2022] Open
Abstract
Plant diseases caused by fungi and oomycetes pose an increasing threat to food security and ecosystem health worldwide. These filamentous pathogens, while taxonomically distinct, modulate host defense responses by secreting effectors, which are typically identified based on the presence of signal peptides. Here we show that Phytophthora sojae and Verticillium dahliae secrete isochorismatases (PsIsc1 and VdIsc1, respectively) that are required for full pathogenesis. PsIsc1 and VdIsc1 can suppress salicylate-mediated innate immunity in planta and hydrolyse isochorismate in vitro. A conserved triad of catalytic residues is essential for both functions. Thus, the two proteins are isochorismatase effectors that disrupt the plant salicylate metabolism pathway by suppressing its precursor. Furthermore, these proteins lack signal peptides, but exhibit characteristics that lead to unconventional secretion. Therefore, this secretion pathway is a novel mechanism for delivering effectors and might play an important role in host–pathogen interactions. Salicylate is a regulator of innate immunity to infection in plants. Here, Liu et al. show that two plant pathogens secrete enzymes that disrupt salicylate biosynthesis and plant immunity, and reveal that these effectors are secreted via an unconventional mechanism.
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Affiliation(s)
- Tingli Liu
- 1] Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China [2] Provincial Key Laboratory of Agrobiology, Jiangsu Academy of Agricultural Sciences, Nanjing 210095, China [3]
| | - Tianqiao Song
- 1] Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China [2]
| | - Xiong Zhang
- Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China
| | - Hongbo Yuan
- Provincial Key Laboratory of Agrobiology, Jiangsu Academy of Agricultural Sciences, Nanjing 210095, China
| | - Liming Su
- Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China
| | - Wanlin Li
- Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China
| | - Jing Xu
- Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China
| | - Shiheng Liu
- State Key Laboratory of Microbial Technology, Shandong University, Jinan 250100, China
| | - Linlin Chen
- Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China
| | - Tianzi Chen
- Provincial Key Laboratory of Agrobiology, Jiangsu Academy of Agricultural Sciences, Nanjing 210095, China
| | - Meixiang Zhang
- Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China
| | - Lichuan Gu
- State Key Laboratory of Microbial Technology, Shandong University, Jinan 250100, China
| | - Baolong Zhang
- Provincial Key Laboratory of Agrobiology, Jiangsu Academy of Agricultural Sciences, Nanjing 210095, China
| | - Daolong Dou
- Department of Plant Pathology, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, China
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21
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Eves-van den Akker S, Lilley CJ, Danchin EGJ, Rancurel C, Cock PJA, Urwin PE, Jones JT. The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes. Genome Biol Evol 2014; 6:2181-94. [PMID: 25123114 PMCID: PMC4202313 DOI: 10.1093/gbe/evu171] [Citation(s) in RCA: 36] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 08/03/2014] [Indexed: 11/14/2022] Open
Abstract
Within the phylum Nematoda, plant-parasitism is hypothesized to have arisen independently on at least four occasions. The most economically damaging plant-parasitic nematode species, and consequently the most widely studied, are those that feed as they migrate destructively through host roots causing necrotic lesions (migratory endoparasites) and those that modify host root tissue to create a nutrient sink from which they feed (sedentary endoparasites). The false root-knot nematode Nacobbus aberrans is the only known species to have both migratory endoparasitic and sedentary endoparasitic stages within its life cycle. Moreover, its sedentary stage appears to have characteristics of both the root-knot and the cyst nematodes. We present the first large-scale genetic resource of any false-root knot nematode species. We use RNAseq to describe relative abundance changes in all expressed genes across the life cycle to provide interesting insights into the biology of this nematode as it transitions between modes of parasitism. A multigene phylogenetic analysis of N. aberrans with respect to plant-parasitic nematodes of all groups confirms its proximity to both cyst and root-knot nematodes. We present a transcriptome-wide analysis of both lateral gene transfer events and the effector complement. Comparing parasitism genes of typical root-knot and cyst nematodes to those of N. aberrans has revealed interesting similarities. Importantly, genes that were believed to be either cyst nematode, or root-knot nematode, "specific" have both been identified in N. aberrans. Our results provide insights into the characteristics of a common ancestor and the evolution of sedentary endoparasitism of plants by nematodes.
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Affiliation(s)
- Sebastian Eves-van den Akker
- Centre for Plant Sciences, University of Leeds, United Kingdom Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, United Kingdom
| | | | - Etienne G J Danchin
- Centre National de la Recherche Scientifique, INRA Institut National de la Recherche Agronomique, UMR 1355, Université de Nice-Sophia Antipolis, Sophia-Antipolis, France
| | - Corinne Rancurel
- Centre National de la Recherche Scientifique, INRA Institut National de la Recherche Agronomique, UMR 1355, Université de Nice-Sophia Antipolis, Sophia-Antipolis, France
| | - Peter J A Cock
- Information and Computational Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, United Kingdom
| | - Peter E Urwin
- Centre for Plant Sciences, University of Leeds, United Kingdom
| | - John T Jones
- Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, United Kingdom
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Kyndt T, Fernandez D, Gheysen G. Plant-parasitic nematode infections in rice: molecular and cellular insights. ANNUAL REVIEW OF PHYTOPATHOLOGY 2014; 52:135-53. [PMID: 24906129 DOI: 10.1146/annurev-phyto-102313-050111] [Citation(s) in RCA: 79] [Impact Index Per Article: 7.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/23/2023]
Abstract
Being one of the major staple foods in the world, and an interesting model monocot plant, rice (Oryza sativa L.) has recently received attention from molecular nematologists studying the cellular and molecular aspects of the interaction between this crop and plant-parasitic nematodes. In this review, we highlight recent advances in this field, with a focus on the best-studied root-knot nematodes. Histological studies have revealed the cellular changes inside root-knot nematode-induced feeding sites, both in the compatible interaction with Oryza sativa and the incompatible interaction with the related species Oryza glaberrima. After comparing the published data from transcriptome analyses, mutant studies, and exogenous hormone applications, we provide a comprehensive model showing the role and interaction of plant hormone pathways in defense of this monocot crop against root nematodes, where jasmonate seems to play a key role. Finally, recent evidence indicates that effectors secreted from rice-infecting nematodes can suppress plant defense.
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Affiliation(s)
- Tina Kyndt
- Department of Molecular Biotechnology, Ghent University, 9000 Ghent, Belgium; ,
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