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Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities

Modern agriculture has influenced plant virus emergence through ecosystem simplification, introduction of new host species, and reduction in crop genetic diversity. Therefore, it is crucial to better understand virus distributions across cultivated and uncultivated communities in agro-ecological int...

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Autores principales: Maclot, François, Debue, Virginie, Malmstrom, Carolyn M., Filloux, Denis, Roumagnac, Philippe, Eck, Mathilde, Tamisier, Lucie, Blouin, Arnaud G., Candresse, Thierry, Massart, Sébastien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100685/
https://www.ncbi.nlm.nih.gov/pubmed/36916941
http://dx.doi.org/10.1128/spectrum.04850-22
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author Maclot, François
Debue, Virginie
Malmstrom, Carolyn M.
Filloux, Denis
Roumagnac, Philippe
Eck, Mathilde
Tamisier, Lucie
Blouin, Arnaud G.
Candresse, Thierry
Massart, Sébastien
author_facet Maclot, François
Debue, Virginie
Malmstrom, Carolyn M.
Filloux, Denis
Roumagnac, Philippe
Eck, Mathilde
Tamisier, Lucie
Blouin, Arnaud G.
Candresse, Thierry
Massart, Sébastien
author_sort Maclot, François
collection PubMed
description Modern agriculture has influenced plant virus emergence through ecosystem simplification, introduction of new host species, and reduction in crop genetic diversity. Therefore, it is crucial to better understand virus distributions across cultivated and uncultivated communities in agro-ecological interfaces, as well as virus exchange among them. Here, we advance fundamental understanding in this area by characterizing the virome of three co-occurring replicated Poaceae community types that represent a gradient of grass species richness and management intensity, from highly managed crop monocultures to little-managed, species-rich grasslands. We performed a large-scale study on 950 wild and cultivated Poaceae over 2 years, combining untargeted virome analysis down to the virus species level with targeted detection of three plant viruses. Deep sequencing revealed (i) a diversified and largely unknown Poaceae virome (at least 51 virus species or taxa), with an abundance of so-called persistent viruses; (ii) an increase of virome richness with grass species richness within the community; (iii) stability of virome richness over time but a large viral intraspecific variability; and (iv) contrasting patterns of virus prevalence, coinfections, and spatial distribution among plant communities and species. Our findings highlight the complex structure of plant virus communities in nature and suggest the influence of anthropogenic management on viral distribution and prevalence. IMPORTANCE Because viruses have been mostly studied in cultivated plants, little is known about virus diversity and ecology in less-managed vegetation or about the influence of human management and agriculture on virome composition. Poaceae (grass family)-dominated communities provide invaluable opportunities to examine these ecological issues, as they are distributed worldwide across agro-ecological gradients, are essential for food security and conservation, and can be infected by numerous viruses. Here, we used multiple levels of analysis that considered plant communities, individual plants, virus species, and haplotypes to broaden understanding of the Poaceae virome and to evaluate host-parasite richness relationships within agro-ecological landscapes in our study area. We emphasized the influence of grass diversity and land use on the composition of viral communities and their life history strategies, and we demonstrated the complexity of plant-virus interactions in less-managed grass communities, such as the higher virus prevalence and overrepresentation of mixed virus infection compared to theoretical predictions.
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spelling pubmed-101006852023-04-14 Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities Maclot, François Debue, Virginie Malmstrom, Carolyn M. Filloux, Denis Roumagnac, Philippe Eck, Mathilde Tamisier, Lucie Blouin, Arnaud G. Candresse, Thierry Massart, Sébastien Microbiol Spectr Research Article Modern agriculture has influenced plant virus emergence through ecosystem simplification, introduction of new host species, and reduction in crop genetic diversity. Therefore, it is crucial to better understand virus distributions across cultivated and uncultivated communities in agro-ecological interfaces, as well as virus exchange among them. Here, we advance fundamental understanding in this area by characterizing the virome of three co-occurring replicated Poaceae community types that represent a gradient of grass species richness and management intensity, from highly managed crop monocultures to little-managed, species-rich grasslands. We performed a large-scale study on 950 wild and cultivated Poaceae over 2 years, combining untargeted virome analysis down to the virus species level with targeted detection of three plant viruses. Deep sequencing revealed (i) a diversified and largely unknown Poaceae virome (at least 51 virus species or taxa), with an abundance of so-called persistent viruses; (ii) an increase of virome richness with grass species richness within the community; (iii) stability of virome richness over time but a large viral intraspecific variability; and (iv) contrasting patterns of virus prevalence, coinfections, and spatial distribution among plant communities and species. Our findings highlight the complex structure of plant virus communities in nature and suggest the influence of anthropogenic management on viral distribution and prevalence. IMPORTANCE Because viruses have been mostly studied in cultivated plants, little is known about virus diversity and ecology in less-managed vegetation or about the influence of human management and agriculture on virome composition. Poaceae (grass family)-dominated communities provide invaluable opportunities to examine these ecological issues, as they are distributed worldwide across agro-ecological gradients, are essential for food security and conservation, and can be infected by numerous viruses. Here, we used multiple levels of analysis that considered plant communities, individual plants, virus species, and haplotypes to broaden understanding of the Poaceae virome and to evaluate host-parasite richness relationships within agro-ecological landscapes in our study area. We emphasized the influence of grass diversity and land use on the composition of viral communities and their life history strategies, and we demonstrated the complexity of plant-virus interactions in less-managed grass communities, such as the higher virus prevalence and overrepresentation of mixed virus infection compared to theoretical predictions. American Society for Microbiology 2023-03-14 /pmc/articles/PMC10100685/ /pubmed/36916941 http://dx.doi.org/10.1128/spectrum.04850-22 Text en Copyright © 2023 Maclot et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Maclot, François
Debue, Virginie
Malmstrom, Carolyn M.
Filloux, Denis
Roumagnac, Philippe
Eck, Mathilde
Tamisier, Lucie
Blouin, Arnaud G.
Candresse, Thierry
Massart, Sébastien
Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities
title Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities
title_full Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities
title_fullStr Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities
title_full_unstemmed Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities
title_short Long-Term Anthropogenic Management and Associated Loss of Plant Diversity Deeply Impact Virome Richness and Composition of Poaceae Communities
title_sort long-term anthropogenic management and associated loss of plant diversity deeply impact virome richness and composition of poaceae communities
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100685/
https://www.ncbi.nlm.nih.gov/pubmed/36916941
http://dx.doi.org/10.1128/spectrum.04850-22
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