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Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest

The root‐knot nematodes are the most devastating worms to worldwide agriculture with Meloidogyne incognita being the most widely distributed and damaging species. This parasitic and ecological success seems surprising given its supposed obligatory clonal reproduction. Clonal reproduction has been su...

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Autores principales: Koutsovoulos, Georgios D., Marques, Eder, Arguel, Marie‐Jeanne, Duret, Laurent, Machado, Andressa C. Z., Carneiro, Regina M. D. G., Kozlowski, Djampa K., Bailly‐Bechet, Marc, Castagnone‐Sereno, Philippe, Albuquerque, Erika V. S., Danchin, Etienne G. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976969/
https://www.ncbi.nlm.nih.gov/pubmed/31993088
http://dx.doi.org/10.1111/eva.12881
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author Koutsovoulos, Georgios D.
Marques, Eder
Arguel, Marie‐Jeanne
Duret, Laurent
Machado, Andressa C. Z.
Carneiro, Regina M. D. G.
Kozlowski, Djampa K.
Bailly‐Bechet, Marc
Castagnone‐Sereno, Philippe
Albuquerque, Erika V. S.
Danchin, Etienne G. J.
author_facet Koutsovoulos, Georgios D.
Marques, Eder
Arguel, Marie‐Jeanne
Duret, Laurent
Machado, Andressa C. Z.
Carneiro, Regina M. D. G.
Kozlowski, Djampa K.
Bailly‐Bechet, Marc
Castagnone‐Sereno, Philippe
Albuquerque, Erika V. S.
Danchin, Etienne G. J.
author_sort Koutsovoulos, Georgios D.
collection PubMed
description The root‐knot nematodes are the most devastating worms to worldwide agriculture with Meloidogyne incognita being the most widely distributed and damaging species. This parasitic and ecological success seems surprising given its supposed obligatory clonal reproduction. Clonal reproduction has been suspected based on cytological observations but, so far, never confirmed by population genomics data. As a species, M. incognita is highly polyphagous with thousands of host plants. However, different M. incognita isolates present distinct and overlapping patterns of host compatibilities. Historically, four “host races” had been defined as a function of ranges of compatible and incompatible plants. In this study, we used population genomics to assess whether (a) reproduction is actually clonal in this species, (b) the host races follow an underlying phylogenetic signal or, rather represent multiple independent transitions, and (c) how genome variations associate with other important biological traits such as the affected crops and geographical distribution. We sequenced the genomes of 11 M. incognita isolates across Brazil that covered the four host races in replicates. By aligning the genomic reads of these isolates to the M. incognita reference genome assembly, we identified point variations. Analysis of linkage disequilibrium and 4‐gametes test showed no evidence for recombination, corroborating the clonal reproduction of M. incognita. The few point variations between the isolates showed no significant association with the host races, the geographical origin of the samples, or the crop on which they have been collected. Addition of isolates from other locations around the world confirmed this lack of underlying phylogenetic signal. This suggests multiple gains and losses of parasitic abilities and adaptations to different environments account for the broad host spectrum and wide geographical distribution of M. incognita and thus to its high economic impact. This surprising adaptability without sex poses both evolutionary and agro‐economic challenges.
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spelling pubmed-69769692020-01-28 Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest Koutsovoulos, Georgios D. Marques, Eder Arguel, Marie‐Jeanne Duret, Laurent Machado, Andressa C. Z. Carneiro, Regina M. D. G. Kozlowski, Djampa K. Bailly‐Bechet, Marc Castagnone‐Sereno, Philippe Albuquerque, Erika V. S. Danchin, Etienne G. J. Evol Appl Original Articles The root‐knot nematodes are the most devastating worms to worldwide agriculture with Meloidogyne incognita being the most widely distributed and damaging species. This parasitic and ecological success seems surprising given its supposed obligatory clonal reproduction. Clonal reproduction has been suspected based on cytological observations but, so far, never confirmed by population genomics data. As a species, M. incognita is highly polyphagous with thousands of host plants. However, different M. incognita isolates present distinct and overlapping patterns of host compatibilities. Historically, four “host races” had been defined as a function of ranges of compatible and incompatible plants. In this study, we used population genomics to assess whether (a) reproduction is actually clonal in this species, (b) the host races follow an underlying phylogenetic signal or, rather represent multiple independent transitions, and (c) how genome variations associate with other important biological traits such as the affected crops and geographical distribution. We sequenced the genomes of 11 M. incognita isolates across Brazil that covered the four host races in replicates. By aligning the genomic reads of these isolates to the M. incognita reference genome assembly, we identified point variations. Analysis of linkage disequilibrium and 4‐gametes test showed no evidence for recombination, corroborating the clonal reproduction of M. incognita. The few point variations between the isolates showed no significant association with the host races, the geographical origin of the samples, or the crop on which they have been collected. Addition of isolates from other locations around the world confirmed this lack of underlying phylogenetic signal. This suggests multiple gains and losses of parasitic abilities and adaptations to different environments account for the broad host spectrum and wide geographical distribution of M. incognita and thus to its high economic impact. This surprising adaptability without sex poses both evolutionary and agro‐economic challenges. John Wiley and Sons Inc. 2019-11-06 /pmc/articles/PMC6976969/ /pubmed/31993088 http://dx.doi.org/10.1111/eva.12881 Text en © 2019 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Koutsovoulos, Georgios D.
Marques, Eder
Arguel, Marie‐Jeanne
Duret, Laurent
Machado, Andressa C. Z.
Carneiro, Regina M. D. G.
Kozlowski, Djampa K.
Bailly‐Bechet, Marc
Castagnone‐Sereno, Philippe
Albuquerque, Erika V. S.
Danchin, Etienne G. J.
Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest
title Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest
title_full Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest
title_fullStr Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest
title_full_unstemmed Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest
title_short Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest
title_sort population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976969/
https://www.ncbi.nlm.nih.gov/pubmed/31993088
http://dx.doi.org/10.1111/eva.12881
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