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Li X, Liu K, Rideout S, Rosso L, Zhang B, Welbaum GE. Seed physiological traits and environmental factors influence seedling establishment of vegetable soybean ( Glycine max L.). FRONTIERS IN PLANT SCIENCE 2024; 15:1344895. [PMID: 38887465 PMCID: PMC11180749 DOI: 10.3389/fpls.2024.1344895] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 11/27/2023] [Accepted: 05/20/2024] [Indexed: 06/20/2024]
Abstract
Edamame (Glycine max (L.) Merr.), a specialty soybean prized for its nutritional value and taste, has witnessed a surge in demand within the U.S. However, subpar seedling stands have hindered its production potential, necessitating increased inputs for farmers. This study aims to uncover potential physiological factors contributing to low seedling emergence in edamame. We conducted comprehensive assessments on thirteen prominent edamame genotypes alongside two food-grade and two grain-type soybean genotypes, focusing on germination and emergence speed in both laboratory and field settings. Additionally, we employed single electrical conductivity tests and identified and quantified seed leachate components to distinguish among soybean types. Furthermore, using a LabField™ simulation table, we examined seed emergence across a wide soil temperature range (5°C to 45°C) for edamame and other soybean types. All seeds were produced under the same environmental conditions, harvested in Fall 2020, and stored under uniform conditions to minimize quality variations. Our findings revealed minimal divergence in emergence percentages among the seventeen genotypes, with over 95% germination and emergence in laboratory conditions and over 70% emergence in the field. Nonetheless, edamame genotypes typically exhibited slower germination speeds and higher leachate exudates containing higher soluble sugars and amino acids. Seed size did not significantly impact total emergence but was negatively correlated with germination and emergence speed, although this effect could be mitigated under complex field conditions. Furthermore, this study proposed differences that distinguish edamame from other soybean types regarding ideal and base temperatures, as well as thermal time. The finds offer valuable insights into edamame establishment, potentially paving the way for supporting local edamame production in the U.S.
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Affiliation(s)
- Xiaoying Li
- School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA, United States
- Department of Horticultural Sciences, Tropical Research and Education Center, University of Florida, Homestead, FL, United States
| | - Kathryn Liu
- School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA, United States
| | - Steven Rideout
- School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA, United States
| | - Luciana Rosso
- School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA, United States
| | - Bo Zhang
- School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA, United States
| | - Gregory E. Welbaum
- School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA, United States
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Olofintila OE, Noel ZA. Soybean and Cotton Spermosphere Soil Microbiome Shows Dominance of Soilborne Copiotrophs. Microbiol Spectr 2023; 11:e0037723. [PMID: 37260391 PMCID: PMC10434258 DOI: 10.1128/spectrum.00377-23] [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: 01/25/2023] [Accepted: 05/14/2023] [Indexed: 06/02/2023] Open
Abstract
The spermosphere is the transient, immediate zone of soil around imbibing and germinating seeds. It represents a habitat where there is contact between seed-associated microbes and soil microbes, but it is studied less than other plant habitats. Previous studies on spermosphere microbiology were primarily culture based or did not sample the spermosphere soil as initially defined in space and time. Thus, the objectives of this study were to develop an efficient strategy to collect spermosphere soils around imbibing soybean and cotton in nonsterile soil and investigate changes in microbial communities. The method employed sufficiently collected spermosphere soil as initially defined in space by constraining the soil sampled with a cork borer and confining the soil to a 12-well microtiter plate. Spermosphere prokaryote composition changed over time and depended on the crop within 6 h after seeds were sown. By 12 to 18 h, crops had unique microbial communities in spermosphere soils. Prokaryote evenness dropped following seed imbibition, with the proliferation of copiotrophic soil bacteria. Due to their long history of plant growth promotion, prokaryote operational taxonomic units (OTUs) in Bacillus, Paenibacillus, Burkholderia, Massilia, Azospirillum, and Pseudomonas were notable organisms enriched. Fungi and prokaryotes were hub taxa in cotton and soybean spermosphere networks. Additionally, the enriched taxa were not hubs in networks, suggesting that other taxa besides those enriched may be important for spermosphere communities. Overall, this study advances knowledge in the assembly of the plant microbiome early in a plant's life, which may have plant health implications in more mature plant growth stages. IMPORTANCE The central hypothesis of this research was that plant species and seed exudate release would alter the assembly of microbes in the spermosphere soil. Our research investigated the response of microbes to the initial burst of nutrients into the spermosphere soil, filling knowledge gaps from previous studies that pregerminated seeds under sterile conditions. We identified several copiotrophic bacterial lineages with a long history of plant growth promotion proliferating in response to the initial exudate release. With a comparative network approach, we show that these copiotrophic bacteria are not central to networks, demonstrating that other microbes (including fungi) may be important for community structure. This study improves knowledge on microbial dynamics in the understudied spermosphere and helps inform solutions for biologically or ecologically motivated solutions to spermosphere pathogens.
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Affiliation(s)
| | - Zachary A. Noel
- Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, USA
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War AF, Bashir I, Reshi ZA, Kardol P, Rashid I. Insights into the seed microbiome and its ecological significance in plant life. Microbiol Res 2023; 269:127318. [PMID: 36753851 DOI: 10.1016/j.micres.2023.127318] [Citation(s) in RCA: 19] [Impact Index Per Article: 9.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/05/2022] [Revised: 12/12/2022] [Accepted: 02/01/2023] [Indexed: 02/05/2023]
Abstract
In recent years, the microbiome has attracted much attention because of the multiple roles and functions that microbes play in plants, animals, and human beings. Seed-associated microbes are of particular interest in being the initial microbial inoculum that affects the critical early life stages of a plant. The seed-microbe interactions are also known to improve nutrient acquisition, resilience against pathogens, and resistance against abiotic stresses. Despite these diverse roles, the seed microbiome has received little attention in plant ecology. Thus, we review the current knowledge on seed microbial diversity, community structure, and functions obtained through culture-dependent and culture-independent approaches. Furthermore, we present a comprehensive synthesis of the ecological literature on seed-microbe interactions to better understand the impact of these interactions on plant health and productivity. We suggest that future research should focus on the role of the seed microbiome in the establishment, colonization and spread of plant species in their native and non-native ranges as it may provide new insights into conservation biology and invasion ecology.
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Affiliation(s)
- Aadil Farooq War
- Department of Botany, University of Kashmir, Srinagar 190006, Jammu and Kashmir, India.
| | - Iqra Bashir
- Department of Botany, University of Kashmir, Srinagar 190006, Jammu and Kashmir, India
| | - Zafar A Reshi
- Department of Botany, University of Kashmir, Srinagar 190006, Jammu and Kashmir, India
| | - Paul Kardol
- Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, S 901 83 Umeå, Sweden
| | - Irfan Rashid
- Department of Botany, University of Kashmir, Srinagar 190006, Jammu and Kashmir, India
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Zhao Y, Yuan Z, Wang S, Wang H, Chao Y, Sederoff RR, Sederoff H, Yan H, Pan J, Peng M, Wu D, Borriss R, Niu B. Gene sdaB Is Involved in the Nematocidal Activity of Enterobacter ludwigii AA4 Against the Pine Wood Nematode Bursaphelenchus xylophilus. Front Microbiol 2022; 13:870519. [PMID: 35602027 PMCID: PMC9121001 DOI: 10.3389/fmicb.2022.870519] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/06/2022] [Accepted: 03/25/2022] [Indexed: 11/13/2022] Open
Abstract
Bursaphelenchus xylophilus, a plant parasitic nematode, is the causal agent of pine wilt, a devastating forest tree disease. Essentially, no efficient methods for controlling B. xylophilus and pine wilt disease have yet been developed. Enterobacter ludwigii AA4, isolated from the root of maize, has powerful nematocidal activity against B. xylophilus in a new in vitro dye exclusion test. The corrected mortality of the B. xylophilus treated by E. ludwigii AA4 or its cell extract reached 98.3 and 98.6%, respectively. Morphological changes in B. xylophilus treated with a cell extract from strain AA4 suggested that the death of B. xylophilus might be caused by an increased number of vacuoles in non-apoptotic cell death and the damage to tissues of the nematodes. In a greenhouse test, the disease index of the seedlings of Scots pine (Pinus sylvestris) treated with the cells of strain AA4 plus B. xylophilus or those treated by AA4 cell extract plus B. xylophilus was 38.2 and 30.3, respectively, was significantly lower than 92.5 in the control plants treated with distilled water and B. xylophilus. We created a sdaB gene knockout in strain AA4 by deleting the gene that was putatively encoding the beta-subunit of L-serine dehydratase through Red homologous recombination. The nematocidal and disease-suppressing activities of the knockout strain were remarkably impaired. Finally, we revealed a robust colonization of P. sylvestris seedling needles by E. ludwigii AA4, which is supposed to contribute to the disease-controlling efficacy of strain AA4. Therefore, E. ludwigii AA4 has significant potential to serve as an agent for the biological control of pine wilt disease caused by B. xylophilus.
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Affiliation(s)
- Yu Zhao
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China
- College of Life Science, Northeast Forestry University, Harbin, China
| | - Zhibo Yuan
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China
- College of Life Science, Northeast Forestry University, Harbin, China
| | - Shuang Wang
- Administrative Office of the Summer Palace, Beijing Municipal Administration Center of Parks, Beijing, China
| | - Haoyu Wang
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China
- College of Life Science, Northeast Forestry University, Harbin, China
| | - Yanjie Chao
- The Center for Microbes, Development and Health (CMDH), Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai, China
| | - Ronald R. Sederoff
- Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC, United States
| | - Heike Sederoff
- Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United States
| | - He Yan
- Center for Biological Disaster Prevention and Control, National Forestry and Grassland Administration, Shenyang, China
| | - Jialiang Pan
- Center for Biological Disaster Prevention and Control, National Forestry and Grassland Administration, Shenyang, China
| | - Mu Peng
- College of Biological Science and Technology, Hubei Minzu University, Enshi, China
| | - Di Wu
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China
- College of Life Science, Northeast Forestry University, Harbin, China
| | - Rainer Borriss
- Nord Reet UG, Greifswald, Germany
- Institute of Marine Biotechnology e.V. (IMaB), Greifswald, Germany
- *Correspondence: Rainer Borriss,
| | - Ben Niu
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China
- College of Life Science, Northeast Forestry University, Harbin, China
- Ben Niu,
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Meena M, Yadav G, Sonigra P, Nagda A, Mehta T, Zehra A, Swapnil P. Role of Microbial Bioagents as Elicitors in Plant Defense Regulation. TRANSCRIPTION FACTORS FOR BIOTIC STRESS TOLERANCE IN PLANTS 2022:103-128. [DOI: 10.1007/978-3-031-12990-2_6] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/18/2023]
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Influence of Salt Stress on Growth of Spermosphere Bacterial Communities in Different Peanut ( Arachis hypogaea L.) Cultivars. Int J Mol Sci 2020; 21:ijms21062131. [PMID: 32244906 PMCID: PMC7139419 DOI: 10.3390/ijms21062131] [Citation(s) in RCA: 12] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/16/2020] [Revised: 03/17/2020] [Accepted: 03/18/2020] [Indexed: 11/17/2022] Open
Abstract
Background: Exposure of seeds to high salinity can cause reduced germination and poor seedling establishment. Improving the salt tolerance of peanut (Arachis hypogaea L.) seeds during germination is an important breeding goal of the peanut industry. Bacterial communities in the spermosphere soils may be of special importance to seed germination under salt stress, whereas extant results in oilseed crop peanut are scarce. Methods: Here, bacterial communities colonizing peanut seeds with salt stress were characterized using 16S rRNA gene sequencing. Results: Peanut spermosphere was composed of four dominant genera: Bacillus, Massilia, Pseudarthrobacter, and Sphingomonas. Comparisons of bacterial community structure revealed that the beneficial bacteria (Bacillus), which can produce specific phosphatases to sequentially mineralize organic phosphorus into inorganic phosphorus, occurred in relatively higher abundance in salt-treated spermosphere soils. Further soil enzyme activity assays showed that phosphatase activity increased in salt-treated spermosphere soils, which may be associated with the shift of Bacillus. Conclusion: This study will form the foundation for future improvement of salt tolerance of peanuts at the seed germination stage via modification of the soil microbes.
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Torres-Cortés G, Bonneau S, Bouchez O, Genthon C, Briand M, Jacques MA, Barret M. Functional Microbial Features Driving Community Assembly During Seed Germination and Emergence. FRONTIERS IN PLANT SCIENCE 2018; 9:902. [PMID: 30008730 PMCID: PMC6034153 DOI: 10.3389/fpls.2018.00902] [Citation(s) in RCA: 46] [Impact Index Per Article: 6.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/08/2018] [Accepted: 06/07/2018] [Indexed: 05/03/2023]
Abstract
Microbial interactions occurring on and around seeds are especially important for plant fitness since seed-borne microorganisms are the initial source of inoculum for the plant microbiota. In this study, we analyze structural and functional changes occurring within the plant microbiota at these early stages of the plant cycle, namely germination and emergence. To this purpose, we performed shotgun DNA sequencing of microbial assemblages associated to seeds, germinating seeds and seedlings of two plant species: bean and radish. We observed an enrichment of Enterobacteriales and Pseudomonadales during emergence and a set of functional traits linked to copiotrophy that could be responsible for this selection as a result of an increase of nutrient availability after germination. Representative bacterial isolates of taxa that are selected in seedlings showed indeed faster bacterial growth rate in comparison to seed-associated bacteria isolates. Finally, binning of metagenomics contigs results in the reconstruction of population genomes of the major bacterial taxa associated to the samples. Together, our results demonstrate that, although seed microbiota varied across plant species, nutrient availability during germination elicits changes of the composition of microbial communities by potentially selecting microbial groups with functional traits linked to copiotrophy. The data presented here represents the first attempts to empirically assess changes in the microbial community during plant emergence and moves us toward a more holistic understanding of the plant microbiome.
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Affiliation(s)
| | - Sophie Bonneau
- IRHS, INRA, Agrocampus Ouest, Université d’Angers, Beaucouzé, France
| | | | | | - Martial Briand
- IRHS, INRA, Agrocampus Ouest, Université d’Angers, Beaucouzé, France
| | | | - Matthieu Barret
- IRHS, INRA, Agrocampus Ouest, Université d’Angers, Beaucouzé, France
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Yamawo A, Mukai H. Seeds integrate biological information about conspecific and allospecific neighbours. Proc Biol Sci 2018. [PMID: 28637859 DOI: 10.1098/rspb.2017.0800] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/21/2022] Open
Abstract
Numerous organisms integrate information from multiple sources and express adaptive behaviours, but how they do so at different developmental stages remains to be identified. Seeds, which are the embryonic stage of plants, need to make decisions about the timing of emergence in response to environmental cues related to survival. We investigated the timing of emergence of Plantago asiatica (Plantaginaceae) seed while manipulating the presence of Trifolium repens seed and the relatedness of neighbouring P. asiatica seed. The relatedness of neighbouring P. asiatica seed and the presence of seeds of T. repens did not on their own influence the timing of P. asiatica emergence. However, when encountering a T. repens seed, a P. asiatica seed emerged faster in the presence of a sibling seed than in the presence of a non-sibling seed. Water extracts of seeds gave the same result. We show that P. asiatica seeds integrate information about the relatedness of neighbouring P. asiatica seeds and the presence of seeds of a different species via water-soluble chemicals and adjust their emergence behaviour in response. These findings suggest the presence of kin-dependent interspecific interactions.
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Affiliation(s)
- Akira Yamawo
- Faculty of Agriculture and Life Science, Hirosaki University, 1, Bunkyo-cho, Hirosaki 036-8560, Japan
| | - Hiromi Mukai
- Department of Forest Entomology, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan
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9
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Transmission of Bacterial Endophytes. Microorganisms 2017; 5:microorganisms5040070. [PMID: 29125552 PMCID: PMC5748579 DOI: 10.3390/microorganisms5040070] [Citation(s) in RCA: 207] [Impact Index Per Article: 25.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/20/2017] [Revised: 11/06/2017] [Accepted: 11/07/2017] [Indexed: 01/02/2023] Open
Abstract
Plants are hosts to complex communities of endophytic bacteria that colonize the interior of both below- and aboveground tissues. Bacteria living inside plant tissues as endophytes can be horizontally acquired from the environment with each new generation, or vertically transmitted from generation to generation via seed. A better understanding of bacterial endophyte transmission routes and modes will benefit studies of plant–endophyte interactions in both agricultural and natural ecosystems. In this review, we provide an overview of the transmission routes that bacteria can take to colonize plants, including vertically via seeds and pollen, and horizontally via soil, atmosphere, and insects. We discuss both well-documented and understudied transmission routes, and identify gaps in our knowledge on how bacteria reach the inside of plants. Where little knowledge is available on endophytes, we draw from studies on bacterial plant pathogens to discuss potential transmission routes. Colonization of roots from soil is the best studied transmission route, and probably the most important, although more studies of transmission to aerial parts and stomatal colonization are needed, as are studies that conclusively confirm vertical transfer. While vertical transfer of bacterial endophytes likely occurs, obligate and strictly vertically transferred symbioses with bacteria are probably unusual in plants. Instead, plants appear to benefit from the ability to respond to a changing environment by acquiring its endophytic microbiome anew with each generation, and over the lifetime of individuals.
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Schiltz S, Gaillard I, Pawlicki-Jullian N, Thiombiano B, Mesnard F, Gontier E. A review: what is the spermosphere and how can it be studied? J Appl Microbiol 2015; 119:1467-81. [PMID: 26332271 DOI: 10.1111/jam.12946] [Citation(s) in RCA: 48] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/19/2015] [Revised: 07/27/2015] [Accepted: 08/15/2015] [Indexed: 11/27/2022]
Abstract
The spermosphere is the zone surrounding seeds where interactions between the soil, microbial communities and germinating seeds take place. The concept of the spermosphere is usually only applied during germination sensu stricto. Despite the transient nature of this very small zone of soil around the germinating seed, the microbial activities which occur there may have long-lasting impacts on plants. The spermosphere is indirectly characterized by either (i) seed exudates, which could be inhibitors or stimulators of micro-organism growth or (ii) the composition of the microbiome on and around the germinating seeds. The microbial communities present in the spermosphere directly reflect that of the germination medium or are host-dependent and influenced quantitatively and qualitatively by host exudates. Despite its strong impact on the future development of plants, the spermosphere remains little studied. This can be explained by the technical difficulties related to characterizing this concept due to its short duration, small size and biomass, and the number and complexity of the interactions that take place. However, recent technical methods, such as metabolite profiling, combining phenotypic methods with DNA- and RNA-based methods, could be used to investigate seed exudates, microbial communities and their interactions with the soil environment.
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Affiliation(s)
- S Schiltz
- Biologie des Plantes et Innovation (BIOPI), Université de Picardie Jules Verne, Amiens, France
| | - I Gaillard
- Biologie des Plantes et Innovation (BIOPI), Université de Picardie Jules Verne, Amiens, France
| | - N Pawlicki-Jullian
- Biologie des Plantes et Innovation (BIOPI), Université de Picardie Jules Verne, Amiens, France
| | - B Thiombiano
- Biologie des Plantes et Innovation (BIOPI), Université de Picardie Jules Verne, Amiens, France
| | - F Mesnard
- Biologie des Plantes et Innovation (BIOPI), Université de Picardie Jules Verne, Amiens, France
| | - E Gontier
- Biologie des Plantes et Innovation (BIOPI), Université de Picardie Jules Verne, Amiens, France
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Selection of potential biological control of Exserohilum turcicum with epiphytic microorganisms from maize. Rev Argent Microbiol 2015; 47:62-71. [PMID: 25771226 DOI: 10.1016/j.ram.2015.01.002] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/09/2014] [Revised: 12/23/2014] [Accepted: 01/05/2015] [Indexed: 11/22/2022] Open
Abstract
The aims of this study were to select microbial isolates from phyllosphere of maize and to examine their antagonistic activity against Exserohilum turcicum. Selection was performed through the ability of isolates to compete with the pathogen using an index of dominance and to affect growth parameters of E. turcicum. Most of the epiphytic populations obtained for the screening were bacteria. These isolates were found in the order of 6 log CFU/g of leaf fresh weight. According to similar morphological characteristics and staining, 44 out of 111 isolates obtained were selected for testing antagonistic effects. At water potential, ψ, -1.38MPa and -4.19MPa, three Bacillus isolates showed dominance at a distance (5/0) and a significant reduction of growth rate of the pathogen. Three Bacillus isolates only decreased the growth rate of E. turcicum at -1.38MPa. At -4.19MPa the growth rate decreased with three isolates of Pantoea and three Bacillus. In this study a negative and significant correlation was observed between the growth rate of E. turcicum and the dominance index in the interaction of the pathogen with some bacteria. These results show that with decreasing growth rate of the pathogen the dominance index of the interaction increases. Eleven potential biocontrol agents against E. turcicum were selected.
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Bahramisharif A, Lamprecht SC, Calitz F, McLeod A. Suppression of Pythium and Phytophthora Damping-Off of Rooibos by Compost and a Combination of Compost and Nonpathogenic Pythium Taxa. PLANT DISEASE 2013; 97:1605-1610. [PMID: 30716850 DOI: 10.1094/pdis-04-13-0360-re] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/09/2023]
Abstract
Pathogenic oomycetes, including Phytophthora cinnamomi and several Pythium spp. (Pythium irregulare, P. mamillatum, P. myriotylum, and P. pyrilobum), cause serious damping-off problems in rooibos (Aspalathus linearis) nurseries. The management of these pathogens in organic nurseries is problematic, because phenylamide fungicides may not be used. Compost, or compost in combination with Pythium taxa that are nonpathogenic to rooibos (P. acanthicum, P. cederbergense, and Pythium RB II), were investigated as alternative management options. Compost was able to suppress damping-off caused by several oomycete isolates but there was within- and between-species variation among the 30 evaluated isolates. This phenomenon was observed using two compost batches (A and B) sourced from independent suppliers. Compost B significantly reduced damping-off caused by 60% of the isolates, whereas compost A controlled only 37% of the isolates. The pathogens that were more readily controlled by both composts included P. mamillatum and P. pyrilobum, whereas the composts were ineffective at suppressing damping-off caused by >62% of P. irregulare and >50% of P. myriotylum isolates. Based on the evaluation of one Phytophthora cinnamomi isolate, this pathogen may also be controlled by compost. Neither of the composts as a stand-alone treatment could suppress damping-off caused by a combination of pathogenic species (P. cinnamomi, Pythium irregulare, P. mamillatum, P. myriotylum, and P. pyrilobum). However, damping-off was significantly reduced when nonpathogenic Pythium taxa (P. acanthicum, P. cederbergense, and Pythium RB II) were combined with the composts. Similarly, damping-off caused by a P. irregulare isolate that was not suppressed by either of the composts alone was significantly suppressed when the two composts were inoculated with the nonpathogenic Pythium taxa.
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Affiliation(s)
- Amirhossein Bahramisharif
- Department of Plant Pathology, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa
| | - Sandra C Lamprecht
- Agricultural Research Council-Plant Protection Research Institute, Private Bag X5017, Stellenbosch 7599, South Africa
| | - Frikkie Calitz
- Agricultural Research Council-Biometry Unit, Pretoria, 0001, South Africa
| | - Adéle McLeod
- Department of Plant Pathology, University of Stellenbosch, South Africa
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Li S, Jin X, Chen J. Effects of piperidine and piperideine alkaloids from the venom of red imported fire ants, Solenopsis invicta Buren, on Pythium ultimum Trow growth in vitro and the application of piperideine alkaloids to control cucumber damping-off in the greenhouse. PEST MANAGEMENT SCIENCE 2012; 68:1546-1552. [PMID: 22685059 DOI: 10.1002/ps.3337] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/23/2011] [Revised: 03/22/2012] [Accepted: 05/02/2012] [Indexed: 06/01/2023]
Abstract
BACKGROUND Pythium ultimum is a plant pathogen that causes significant yield losses on many economically important crops. Chemical treatment has been used for disease control. In searching for alternatives, venom piperidine and piperideine alkaloids from red imported fire ants were tested against P. ultimum in vitro, and piperideines were employed to control cucumber damping-off in the greenhouse as drench treatments. Results Piperidine and piperideine alkaloids of the red imported fire ant significantly inhibited mycelium growth of P. ultimum. Piperidine alkaloids were stable at both room and elevated temperatures. The inhibitory activity positively correlated with the concentrations of piperidine alkaloids in the medium, and the EC(50) = 17.0 µg ml(-1). Germination of sporangia of P. ultimum was negatively correlated with the concentrations of piperidine alkaloids in the medium, and the EC(50) = 12.3 µg ml(-1). The piperideine alkaloid drenching treatment significantly improved seedling emergence and seedling height of cucumber. CONCLUSION This is the first report describing the use of venom alkaloids from the red imported fire ant to inhibit P. ultimum in the laboratory and the application of piperideine alkaloids to control damping-off disease caused by P. ultimum in the greenhouse. These findings may lead to the development of a new group of fungicides.
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Affiliation(s)
- Shezeng Li
- Institute of Plant Protection, Hebei Academy of Agricultural and Forestry Sciences, Baoding, Hebei Province, China
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Chen MH, Nelson EB. Microbial-induced carbon competition in the spermosphere leads to pathogen and disease suppression in a municipal biosolids compost. PHYTOPATHOLOGY 2012; 102:588-596. [PMID: 22352306 DOI: 10.1094/phyto-08-11-0241] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/31/2023]
Abstract
The aim of this study was to understand whether competition for fatty acids in plant seed exudates by compost-derived seed-colonizing microbial communities could explain the suppression of plant infections initiated by sporangia of Pythium ultimum. The germination behavior of P. ultimum sporangia in response to cucumber seeds was measured to determine the impact of seed-colonizing microbes on pathogen suppression. Seed-colonizing microbial communities from municipal biosolids compost utilized cucumber seed exudates and linoleic acid in vitro, reducing the respective stimulatory activity of these elicitors to P. ultimum sporangial germination. However, when sporangia were observed directly in the spermosphere of seeds sown in the compost medium, levels of germination and sporangial emptying did not differ from the responses in sand. The percentage of aborted germ tubes was greater after incubating sporangia in compost medium for 12-h than the level of germ tube abortion when sporangia were incubated in sand. Abortion did not occur if previously germinated sporangia were supplemented with cucumber seed exudate. Furthermore, removal of cucumber seed exudate after various stages of germ tube emergence resulted in an increase in aborted germ tubes over time. Adding increasing levels of glucose directly to the compost medium alleviated germ tube abortion in the spermosphere and also eliminated disease suppression. These data fail to support a role for linoleic acid competition in Pythium seedling disease suppression but provide evidence for general carbon competition mediated by seed-colonizing microbial communities as a mechanism for the suppression of Pythium seed infections in municipal biosolids compost.
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Affiliation(s)
- Mei-Hsing Chen
- Cornell University, Department of Plant Pathology and Plant-Microbe Biology, 334 Plant Science Building, Ithaca, NY 14853-4203, USA
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Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 2012; 7:e30438. [PMID: 22363438 PMCID: PMC3281832 DOI: 10.1371/journal.pone.0030438] [Citation(s) in RCA: 242] [Impact Index Per Article: 18.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/08/2011] [Accepted: 12/20/2011] [Indexed: 11/30/2022] Open
Abstract
Bacterial endophytes are ubiquitous to virtually all terrestrial plants. With the increasing appreciation of studies that unravel the mutualistic interactions between plant and microbes, we increasingly value the beneficial functions of endophytes that improve plant growth and development. However, still little is known on the source of established endophytes as well as on how plants select specific microbial communities to establish associations. Here, we used cultivation-dependent and -independent approaches to assess the endophytic bacterrial community of surface-sterilized rice seeds, encompassing two consecutive rice generations. We isolated members of nine bacterial genera. In particular, organisms affiliated with Stenotrophomonas maltophilia and Ochrobactrum spp. were isolated from both seed generations. PCR-based denaturing gradient gel electrophoresis (PCR-DGGE) of seed-extracted DNA revealed that approximately 45% of the bacterial community from the first seed generation was found in the second generation as well. In addition, we set up a greenhouse experiment to investigate abiotic and biotic factors influencing the endophytic bacterial community structure. PCR-DGGE profiles performed with DNA extracted from different plant parts showed that soil type is a major effector of the bacterial endophytes. Rice plants cultivated in neutral-pH soil favoured the growth of seed-borne Pseudomonas oryzihabitans and Rhizobium radiobacter, whereas Enterobacter-like and Dyella ginsengisoli were dominant in plants cultivated in low-pH soil. The seed-borne Stenotrophomonas maltophilia was the only conspicuous bacterial endophyte found in plants cultivated in both soils. Several members of the endophytic community originating from seeds were observed in the rhizosphere and surrounding soils. Their impact on the soil community is further discussed.
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Heydari A, Pessarakli M. A Review on Biological Control of Fungal Plant Pathogens Using Microbial Antagonists. ACTA ACUST UNITED AC 2010. [DOI: 10.3923/jbs.2010.273.290] [Citation(s) in RCA: 145] [Impact Index Per Article: 9.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/15/2022]
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Metabolic behavior of bacterial biological control agents in soil and plant rhizospheres. ADVANCES IN APPLIED MICROBIOLOGY 2008; 65:199-215. [PMID: 19026866 DOI: 10.1016/s0065-2164(08)00607-2] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/23/2022]
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Chen MH, Nelson EB. Seed-colonizing microbes from municipal biosolids compost suppress Pythium ultimum damping-off on different plant species. PHYTOPATHOLOGY 2008; 98:1012-8. [PMID: 18943739 DOI: 10.1094/phyto-98-9-1012] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/24/2023]
Abstract
Composts are known for their suppressive properties toward many different seed- and root-infecting pathogens and diseases. Although disease and pathogen suppression induced by composts is believed to be mediated by microbial activities, the nature of the microbial species and processes responsible for suppressiveness remain unknown. We demonstrated previously that seed-colonizing microbial consortia from leaf compost could explain the observed levels of Pythium ultimum-induced damping-off suppression on cotton. The aim of the present work was to determine whether seed-colonizing microbial consortia could explain Pythium damping-off suppression in municipal biosolids compost on three different plant species. Significant levels of disease suppression were observed on cucumber, wheat, and pea at water potentials of -2 kPa. The suppression of damping-off on cucumber and wheat could be eliminated by autoclaving the compost prior to sowing. High levels of suppressiveness were expressed both on cucumber and on wheat seed surfaces within 8 h of sowing. However, the expression of damping-off suppression on the surface of pea seeds was inconsistent and highly variable. Our results demonstrate that compost-induced suppression of P. ultimum damping-off of cucumber and wheat can be explained by the microbial consortia colonizing seeds within 8 h of sowing. These results further suggest that disease suppression in composts is related to microbial species that interact with the pathogen in its infection court and not in the bulk compost.
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Affiliation(s)
- M-H Chen
- Cornell University, Department of Plant Pathology and Plant-Microbe Biology, Ithaca, NY 14853-4203, USA
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Minerdi D, Moretti M, Gilardi G, Barberio C, Gullino ML, Garibaldi A. Bacterial ectosymbionts and virulence silencing in a Fusarium oxysporum strain. Environ Microbiol 2008; 10:1725-41. [DOI: 10.1111/j.1462-2920.2008.01594.x] [Citation(s) in RCA: 67] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
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Temporal release of fatty acids and sugars in the spermosphere: impacts on Enterobacter cloacae-induced biological control. Appl Environ Microbiol 2008; 74:4292-9. [PMID: 18515478 DOI: 10.1128/aem.00264-08] [Citation(s) in RCA: 15] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022] Open
Abstract
The aim of this study was to determine the temporal release of fatty acids and sugars from corn and cucumber seeds during the early stages of seed germination in order to establish whether sugars found in exudate can prevent exudate fatty acid degradation by Enterobacter cloacae. Both saturated (long-chain saturated fatty acids [LCSFA]) and unsaturated (long-chain unsaturated fatty acids [LCUFA]) fatty acids were detected in corn and cucumber seed exudates within 15 min after seed sowing. LCSFA and LCUFA were released at a rate of 26.1 and 6.44 ng/min/seed by corn and cucumber seeds, respectively. The unsaturated portion of the total fatty acid pool from both plant species contained primarily oleic and linoleic acids, and these fatty acids were released at a combined rate of 6.6 and 0.67 ng/min/seed from corn and cucumber, respectively. In the absence of seed exudate sugars, E. cloacae degraded linoleic acid at rates of 29 to 39 ng/min, exceeding the rate of total fatty acid release from seeds. Sugars constituted a significant percentage of corn seed exudate, accounting for 41% of the total dry seed weight. Only 5% of cucumber seed exudate was comprised of sugars. Glucose, fructose, and sucrose were the most abundant sugars present in seed exudate from both plant species. Corn seeds released a total of 137 microg/seed of these three sugars within 30 min of sowing, whereas cucumber seeds released 0.83 microg/seed within the same time frame. Levels of glucose, fructose, and sucrose found in corn seed exudate (90 to 342 microg) reduced the rate of linoleic acid degradation by E. cloacae to 7.5 to 8.8 ng/min in the presence of either sugar, leaving sufficient concentrations of linoleic acid to activate Pythium ultimum sporangia Our results demonstrate that elevated levels of sugars in the corn spermosphere can prevent the degradation of LCUFA by E. cloacae, leading to its failure to suppress P. ultimum sporangial activation, germination, and subsequent disease development.
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Differential interference with Pythium ultimum sporangial activation and germination by Enterobacter cloacae in the corn and cucumber spermospheres. Appl Environ Microbiol 2008; 74:4285-91. [PMID: 18515482 DOI: 10.1128/aem.00263-08] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022] Open
Abstract
Differential protection of plants by Enterobacter cloacae was studied by investigating early sensing and response behavior of Pythium ultimum sporangia toward seeds in the presence or absence of E. cloacae. Ten percent of P. ultimum sporangia were activated within the first 30 min of exposure to cucumber seeds. In contrast, 44% of the sporangia were activated as early as 15 min after exposure to corn seeds with over 80% sporangial activation by 30 min. Germ tubes emerged from sporangia after 2.5 and 1.0 h in the cucumber and corn spermospheres, respectively. Seed application of the wild-type strain of E. cloacae (EcCT-501R3) reduced sporangial activation by 45% in the cucumber spermosphere, whereas no reduction was observed in the corn spermosphere. Fatty acid transport and degradation mutants of E. cloacae (strains EcL1 and Ec31, respectively) did not reduce sporangial activation in either of the spermospheres. Although wild-type or mutant strains of E. cloacae failed to reduce seed colonization incidence, pathogen biomass on cucumber seeds was reduced in the presence of E. cloacae strains EcCT-501R3 and Ec31 by 4 and 8 h after sowing, respectively. By 12 h, levels of P. ultimum on cucumber seeds treated with E. cloacae EcCT-501R3 did not differ from levels on noninoculated seeds. On corn seeds, P. ultimum biomass was not affected by the presence of any E. cloacae strain. When introduced after sporangial activation had occurred, E. cloacae failed to reduce P. ultimum biomass on cucumber seeds compared with that on nontreated seeds. Also, increasing numbers of sporangia used to inoculate seeds yielded increased pathogen biomass at each sampling time. This indicates a direct link between the level of seed-colonizing biomass of P. ultimum and the number of activated and germinated sporangia in the spermosphere, suggesting that E. cloacae suppresses P. ultimum seed infections by reducing sporangial activation and germination within the first 30 to 90 min after sowing.
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Rudrappa T, Biedrzycki ML, Bais HP. Causes and consequences of plant-associated biofilms. FEMS Microbiol Ecol 2008; 64:153-66. [PMID: 18355294 DOI: 10.1111/j.1574-6941.2008.00465.x] [Citation(s) in RCA: 91] [Impact Index Per Article: 5.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2022] Open
Abstract
The rhizosphere is the critical interface between plant roots and soil where beneficial and harmful interactions between plants and microorganisms occur. Although microorganisms have historically been studied as planktonic (or free-swimming) cells, most are found attached to surfaces, in multicellular assemblies known as biofilms. When found in association with plants, certain bacteria such as plant growth promoting rhizobacteria not only induce plant growth but also protect plants from soil-borne pathogens in a process known as biocontrol. Contrastingly, other rhizobacteria in a biofilm matrix may cause pathogenesis in plants. Although research suggests that biofilm formation on plants is associated with biological control and pathogenic response, little is known about how plants regulate this association. Here, we assess the biological importance of biofilm association on plants.
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Affiliation(s)
- Thimmaraju Rudrappa
- Department of Plant and Soil Sciences, University of Delaware, Newark, DE 19711, USA
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Yu XP, Zhu JL, Yao XP, He SC, Huang HN, Chen WL, Hu YH, Li DB. Identification of anrF gene, a homology of admM of andrimid biosynthetic gene cluster related to the antagonistic activity of Enterobacter cloacae B8. World J Gastroenterol 2005; 11:6152-8. [PMID: 16273642 PMCID: PMC4436632 DOI: 10.3748/wjg.v11.i39.6152] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/24/2005] [Revised: 04/08/2005] [Accepted: 04/11/2005] [Indexed: 02/06/2023] Open
Abstract
AIM To identify the gene (s) related to the antagonistic activity of Enterobacter cloacae B8 and to elucidate its antagonistic mechanism. METHODS Transposon-mediated mutagenesis and tagging method and cassette PCR-based chromosomal walking method were adopted to isolate the mutant strain(s) of B8 that lost the antagonistic activity and to clone DNA fragments around Tn5 insertion site. Sequence compiling and open reading frame (ORF) finding were done with DNAStar program and homologous sequence and conserved domain searches were performed with BlastN or BlastP programs at www.ncbi.nlm.nih.gov. To verify the gene involved in the antagonistic activity, complementation of a full-length clone of the anrF gene to the mutant B8F strain was used. RESULTS A 3 321 bp contig around the Tn5 insertion site was obtained and an ORF of 2 634 bp in length designated as anrF gene encoding for a 877 aa polyketide synthase-like protein was identified. It had a homology of 83% at the nucleotide level and 79% ID/87% SIM at the protein level, to the admM gene of Pantoea agglomerans andrimid biosynthetic gene cluster (AY192157). The Tn5 was inserted at 2 420 bp of the gene corresponding to the COG3319 (the thioesterase domain of type I polyketide synthase) coding region on B8F. The antagonistic activity against Xanthomonas oryzae pv. oryzae was resumed with complementation of the full-length anrF gene to the mutant B8F. CONCLUSION The anrF gene obtained is related to the antagonistic activity of B8, and the antagonistic substances produced by B8 are andrimid and/or its analogs.
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Affiliation(s)
- Xu-Ping Yu
- Veterinary Medicine Department, Animal Science College, Zhejiang University, Hangzhou 310029, Zhejiang Province, China.
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Abstract
The spermosphere represents a short-lived, rapidly changing, and microbiologically dynamic zone of soil surrounding a germinating seed. It is analogous to the rhizosphere, being established largely by the carbon compounds released into the soil once the seed begins to hydrate. These seed exudations drive the microbial activities that take place in the spermosphere, many of which can have long-lasting impacts on plant growth and development as well as on plant health. In this review, I discuss the nature of the spermosphere habitat and the factors that give rise to its character, with emphasis on the types of microbial activities in the spermosphere that have important implications for disease development and biological disease control. This review, which represents the first comprehensive synthesis of the literature on spermosphere biology, is meant to illustrate the unique nature of the spermosphere and how studies of interactions in this habitat may serve as useful experimental models for testing hypotheses about plant-microbe associations and microbial ecology.
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Affiliation(s)
- Eric B Nelson
- Department of Plant Pathology, Cornell University, Ithaca, New York 14853, USA.
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