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Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications

Simultaneous infection of a single plant by various pathogen species is increasingly recognized as an important modulator of host resistance and a driver of pathogen evolution. Because plants in agro-ecosystems are the target of a multitude of pathogenic microbes, co-infection could be frequent, and...

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Autores principales: Tollenaere, Charlotte, Lacombe, Severine, Wonni, Issa, Barro, Mariam, Ndougonna, Cyrielle, Gnacko, Fatoumata, Sérémé, Drissa, Jacobs, Jonathan M., Hebrard, Eugénie, Cunnac, Sebastien, Brugidou, Christophe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5410622/
https://www.ncbi.nlm.nih.gov/pubmed/28507553
http://dx.doi.org/10.3389/fpls.2017.00645
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author Tollenaere, Charlotte
Lacombe, Severine
Wonni, Issa
Barro, Mariam
Ndougonna, Cyrielle
Gnacko, Fatoumata
Sérémé, Drissa
Jacobs, Jonathan M.
Hebrard, Eugénie
Cunnac, Sebastien
Brugidou, Christophe
author_facet Tollenaere, Charlotte
Lacombe, Severine
Wonni, Issa
Barro, Mariam
Ndougonna, Cyrielle
Gnacko, Fatoumata
Sérémé, Drissa
Jacobs, Jonathan M.
Hebrard, Eugénie
Cunnac, Sebastien
Brugidou, Christophe
author_sort Tollenaere, Charlotte
collection PubMed
description Simultaneous infection of a single plant by various pathogen species is increasingly recognized as an important modulator of host resistance and a driver of pathogen evolution. Because plants in agro-ecosystems are the target of a multitude of pathogenic microbes, co-infection could be frequent, and consequently important to consider. This is particularly true for rapidly intensifying crops, such as rice in Africa. This study investigated potential interactions between pathogens causing two of the major rice diseases in Africa: the Rice yellow mottle virus (RYMV) and the bacterium Xanthomonas oryzae pathovar oryzicola (Xoc) in order to: 1/ document virus-bacteria co-infection in rice in the field, 2/ explore experimentally their consequences in terms of symptom development and pathogen multiplication, 3/ test the hypothesis of underlying molecular mechanisms of interactions and 4/ explore potential evolutionary consequences. Field surveys in Burkina Faso revealed that a significant proportion of rice fields were simultaneously affected by the two diseases. Co-infection leads to an increase in bacterial specific symptoms, while a decrease in viral load is observed compared to the mono-infected mock. The lack of effect found when using a bacterial mutant for an effector specifically inducing expression of a small RNA regulatory protein, HEN1, as well as a viral genotype-specific effect, both suggest a role for gene silencing mechanisms mediating the within-plant interaction between RYMV and Xoc. Potential implications for pathogen evolution could not be inferred because genotype-specific effects were found only for pathogens originating from different countries, and consequently not meeting in the agrosystem. We argue that pathogen-pathogen-host interactions certainly deserve more attention, both from a theoretical and applied point of view.
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spelling pubmed-54106222017-05-15 Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications Tollenaere, Charlotte Lacombe, Severine Wonni, Issa Barro, Mariam Ndougonna, Cyrielle Gnacko, Fatoumata Sérémé, Drissa Jacobs, Jonathan M. Hebrard, Eugénie Cunnac, Sebastien Brugidou, Christophe Front Plant Sci Plant Science Simultaneous infection of a single plant by various pathogen species is increasingly recognized as an important modulator of host resistance and a driver of pathogen evolution. Because plants in agro-ecosystems are the target of a multitude of pathogenic microbes, co-infection could be frequent, and consequently important to consider. This is particularly true for rapidly intensifying crops, such as rice in Africa. This study investigated potential interactions between pathogens causing two of the major rice diseases in Africa: the Rice yellow mottle virus (RYMV) and the bacterium Xanthomonas oryzae pathovar oryzicola (Xoc) in order to: 1/ document virus-bacteria co-infection in rice in the field, 2/ explore experimentally their consequences in terms of symptom development and pathogen multiplication, 3/ test the hypothesis of underlying molecular mechanisms of interactions and 4/ explore potential evolutionary consequences. Field surveys in Burkina Faso revealed that a significant proportion of rice fields were simultaneously affected by the two diseases. Co-infection leads to an increase in bacterial specific symptoms, while a decrease in viral load is observed compared to the mono-infected mock. The lack of effect found when using a bacterial mutant for an effector specifically inducing expression of a small RNA regulatory protein, HEN1, as well as a viral genotype-specific effect, both suggest a role for gene silencing mechanisms mediating the within-plant interaction between RYMV and Xoc. Potential implications for pathogen evolution could not be inferred because genotype-specific effects were found only for pathogens originating from different countries, and consequently not meeting in the agrosystem. We argue that pathogen-pathogen-host interactions certainly deserve more attention, both from a theoretical and applied point of view. Frontiers Media S.A. 2017-05-01 /pmc/articles/PMC5410622/ /pubmed/28507553 http://dx.doi.org/10.3389/fpls.2017.00645 Text en Copyright © 2017 Tollenaere, Lacombe, Wonni, Barro, Ndougonna, Gnacko, Sérémé, Jacobs, Hebrard, Cunnac and Brugidou. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Tollenaere, Charlotte
Lacombe, Severine
Wonni, Issa
Barro, Mariam
Ndougonna, Cyrielle
Gnacko, Fatoumata
Sérémé, Drissa
Jacobs, Jonathan M.
Hebrard, Eugénie
Cunnac, Sebastien
Brugidou, Christophe
Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications
title Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications
title_full Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications
title_fullStr Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications
title_full_unstemmed Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications
title_short Virus-Bacteria Rice Co-Infection in Africa: Field Estimation, Reciprocal Effects, Molecular Mechanisms, and Evolutionary Implications
title_sort virus-bacteria rice co-infection in africa: field estimation, reciprocal effects, molecular mechanisms, and evolutionary implications
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5410622/
https://www.ncbi.nlm.nih.gov/pubmed/28507553
http://dx.doi.org/10.3389/fpls.2017.00645
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