Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale

Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information abou...

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Vydáno v:	The ISME Journal Ročník 12; číslo 1; s. 173 - 184
Hlavní autoři:	Bernardo, Pauline, Charles-Dominique, Tristan, Barakat, Mohamed, Ortet, Philippe, Fernandez, Emmanuel, Filloux, Denis, Hartnady, Penelope, Rebelo, Tony A, Cousins, Stephen R, Mesleard, François, Cohez, Damien, Yavercovski, Nicole, Varsani, Arvind, Harkins, Gordon W, Peterschmitt, Michel, Malmstrom, Carolyn M, Martin, Darren P, Roumagnac, Philippe
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	London Nature Publishing Group UK 01.01.2018 Oxford University Press Nature Publishing Group
Témata:	631/326/596/2142 704/158/855 Agricultural land Agriculture Biodiversity Biodiversity hot spots Biomedical and Life Sciences Contact potentials Ecological effects Ecology Ecosystems Environmental Sciences Evolutionary Biology Human influences Information systems Interfaces Land use Life Sciences Luminance distribution Microbial Ecology Microbial Genetics and Genomics Microbiology Original original-article Plant diseases Plant viruses Plants (botany) Population genetics Rivers Viruses
ISSN:	1751-7362, 1751-7370, 1751-7370
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Abstract	Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km 2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8–35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature.
AbstractList	Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8-35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature.Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8-35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature. Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8-35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature. Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8–35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature. Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km 2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8–35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature. Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plant-associated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km 2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8–35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature.
Author	Filloux, Denis Roumagnac, Philippe Bernardo, Pauline Peterschmitt, Michel Yavercovski, Nicole Mesleard, François Charles-Dominique, Tristan Cousins, Stephen R Varsani, Arvind Harkins, Gordon W Fernandez, Emmanuel Rebelo, Tony A Hartnady, Penelope Ortet, Philippe Cohez, Damien Martin, Darren P Barakat, Mohamed Malmstrom, Carolyn M
Author_xml	– sequence: 1 givenname: Pauline surname: Bernardo fullname: Bernardo, Pauline organization: CIRAD, UMR BGPI, BGPI, CIRAD, INRA, Montpellier SupAgro, Univ Montpellier, Department of Plant Biology, Michigan State University, East Lansing, Department of Plant Pathology, Ohio State University, OARDC – sequence: 2 givenname: Tristan surname: Charles-Dominique fullname: Charles-Dominique, Tristan organization: Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Center for Integrative Conservation, Community Ecology and Conservation, Menglun, South African National Biodiversity Institute, Kirstenbosch Research Centre – sequence: 3 givenname: Mohamed surname: Barakat fullname: Barakat, Mohamed organization: CEA, CNRS, Aix-Marseille Université, UMR 7265, LEMIRE – sequence: 4 givenname: Philippe surname: Ortet fullname: Ortet, Philippe organization: CEA, CNRS, Aix-Marseille Université, UMR 7265, LEMIRE – sequence: 5 givenname: Emmanuel surname: Fernandez fullname: Fernandez, Emmanuel organization: CIRAD, UMR BGPI, BGPI, CIRAD, INRA, Montpellier SupAgro, Univ Montpellier – sequence: 6 givenname: Denis surname: Filloux fullname: Filloux, Denis organization: CIRAD, UMR BGPI, BGPI, CIRAD, INRA, Montpellier SupAgro, Univ Montpellier – sequence: 7 givenname: Penelope surname: Hartnady fullname: Hartnady, Penelope organization: Computational Biology Division, Department of Integrative Biomedical Sciences, Institute of Infectious Diseases and Molecular Medicine. University of Cape Town, Observatory – sequence: 8 givenname: Tony A surname: Rebelo fullname: Rebelo, Tony A organization: South African National Biodiversity Institute, Kirstenbosch Research Centre – sequence: 9 givenname: Stephen R surname: Cousins fullname: Cousins, Stephen R organization: South African National Biodiversity Institute, Kirstenbosch Research Centre – sequence: 10 givenname: François surname: Mesleard fullname: Mesleard, François organization: Tour du Valat, Institut de recherche pour la conservation des zones humides méditerranéennes, Institut Méditerranéen de Biodiversité et Ecologie (IMBE), UMR CNRS 7263-IRD 237, Université d'Avignon et des pays du Vaucluse, Aix-Marseille Université, IUT d’Avignon – sequence: 11 givenname: Damien surname: Cohez fullname: Cohez, Damien organization: Tour du Valat, Institut de recherche pour la conservation des zones humides méditerranéennes – sequence: 12 givenname: Nicole surname: Yavercovski fullname: Yavercovski, Nicole organization: Tour du Valat, Institut de recherche pour la conservation des zones humides méditerranéennes – sequence: 13 givenname: Arvind orcidid: 0000-0003-4111-2415 surname: Varsani fullname: Varsani, Arvind organization: The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, School of Biological Sciences and Biomolecular Interaction Centre, University of Canterbury, Structural Biology Research Unit, University of Cape Town, Observatory – sequence: 14 givenname: Gordon W surname: Harkins fullname: Harkins, Gordon W organization: South African Medical Research Council Bioinformatics Unit, South African National Bioinformatics Institute, University of the Western Cape – sequence: 15 givenname: Michel surname: Peterschmitt fullname: Peterschmitt, Michel organization: CIRAD, UMR BGPI, BGPI, CIRAD, INRA, Montpellier SupAgro, Univ Montpellier – sequence: 16 givenname: Carolyn M surname: Malmstrom fullname: Malmstrom, Carolyn M organization: Department of Plant Biology, Michigan State University, East Lansing, Graduate Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing – sequence: 17 givenname: Darren P surname: Martin fullname: Martin, Darren P organization: Computational Biology Division, Department of Integrative Biomedical Sciences, Institute of Infectious Diseases and Molecular Medicine. University of Cape Town, Observatory – sequence: 18 givenname: Philippe surname: Roumagnac fullname: Roumagnac, Philippe email: philippe.roumagnac@cirad.fr organization: CIRAD, UMR BGPI, BGPI, CIRAD, INRA, Montpellier SupAgro, Univ Montpellier
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/29053145$$D View this record in MEDLINE/PubMed https://univ-avignon.hal.science/hal-01790932$$DView record in HAL
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SubjectTerms	631/326/596/2142 704/158/855 Agricultural land Agriculture Biodiversity Biodiversity hot spots Biomedical and Life Sciences Contact potentials Ecological effects Ecology Ecosystems Environmental Sciences Evolutionary Biology Human influences Information systems Interfaces Land use Life Sciences Luminance distribution Microbial Ecology Microbial Genetics and Genomics Microbiology Original original-article Plant diseases Plant viruses Plants (botany) Population genetics Rivers Viruses
Title	Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale
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