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

View ORCID ProfileGeorgios D. Koutsovoulos, Eder Marques, Marie-Jeanne Arguel, Laurent Duret, Andressa C.Z. Machado, Regina M.D.G. Carneiro, Djampa K. Kozlowski, Marc Bailly-Bechet, View ORCID ProfilePhilippe Castagnone-Sereno, View ORCID ProfileErika V.S. Albuquerque, View ORCID ProfileEtienne G.J. Danchin
doi: https://doi.org/10.1101/362129
Georgios D. Koutsovoulos
1INRA, CNRS, Université Côte d’Azur, ISA, Sophia Antipolis, France
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  • ORCID record for Georgios D. Koutsovoulos
Eder Marques
2Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brasil
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Marie-Jeanne Arguel
3CNRS, Université Côte d’Azur, IPMC, France
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Laurent Duret
4Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, F-69100, Villeurbanne, France
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Andressa C.Z. Machado
5Área de Proteção de Plantas, Instituto Agronômico do Paraná, Londrina, Paraná, Brasil
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Regina M.D.G. Carneiro
2Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brasil
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Djampa K. Kozlowski
1INRA, CNRS, Université Côte d’Azur, ISA, Sophia Antipolis, France
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Marc Bailly-Bechet
1INRA, CNRS, Université Côte d’Azur, ISA, Sophia Antipolis, France
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Philippe Castagnone-Sereno
1INRA, CNRS, Université Côte d’Azur, ISA, Sophia Antipolis, France
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  • ORCID record for Philippe Castagnone-Sereno
Erika V.S. Albuquerque
2Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brasil
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  • ORCID record for Erika V.S. Albuquerque
Etienne G.J. Danchin
1INRA, CNRS, Université Côte d’Azur, ISA, Sophia Antipolis, France
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  • ORCID record for Etienne G.J. Danchin
  • For correspondence: etienne.danchin@inra.fr
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ABSTRACT

The most devastating nematodes to worldwide agriculture are the root-knot nematodes with Meloidogyne incognita being the most widely distributed and damaging species. This parasitic and ecological success seem 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. At the species level, M. incognita is highly polyphagous with thousands of host plants. However, the host range varies among different M. incognita isolates that may present distinct and more restricted host compatibilities. Historically, four ‘host races’ had been defined as a function of ranges of compatible and incompatible plants. We sequenced the genomes of 11 isolates across Brazil, covering these four distinct races to assess (i) how clonal reproduction is and (ii) how the level of genome variability associates with biological traits such as the host races, affected agronomic culture, and geographical distribution. By aligning the genomic reads of the isolates to the M. incognita reference genome assembly, we identified SNV and small-scale insertions/deletions. Analysis of linkage disequilibrium and 4-gametes test, showed no sign of recombination, confirming the clonal mode of reproduction of M. incognita. We showed that there are relatively few point variations between the different isolates, and these variations show no significant association with either the host races, the geographical origin of the samples or the host plant on which they have been collected. Due to the lack of phylogenetic signal underlying their existence, we recommend the discontinuation of the terminology ‘race’. Overall, these results suggest that multiple gains and losses of parasitic abilities and adaptations to different environmental conditions account for the broad host spectrum and wide geographic distribution of M. incognita. Hence, this nematode constitutes a model species to study adaptability without sexual recombination and overall low genomic variations in animals.

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  • This version has been peer-reviewed and recommended by Peer Community in Evolutionary Biology. The manuscript has been formatted according to the style, recommendations and template of PCI EVolutionary Biology

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Posted July 09, 2019.
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Population genomics supports clonal reproduction and multiple gains and losses of parasitic abilities in the most devastating nematode plant pest
Georgios D. Koutsovoulos, Eder Marques, Marie-Jeanne Arguel, Laurent Duret, Andressa C.Z. Machado, Regina M.D.G. Carneiro, Djampa K. Kozlowski, Marc Bailly-Bechet, Philippe Castagnone-Sereno, Erika V.S. Albuquerque, Etienne G.J. Danchin
bioRxiv 362129; doi: https://doi.org/10.1101/362129
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Population genomics supports clonal reproduction and multiple gains and losses of parasitic abilities in the most devastating nematode plant pest
Georgios D. Koutsovoulos, Eder Marques, Marie-Jeanne Arguel, Laurent Duret, Andressa C.Z. Machado, Regina M.D.G. Carneiro, Djampa K. Kozlowski, Marc Bailly-Bechet, Philippe Castagnone-Sereno, Erika V.S. Albuquerque, Etienne G.J. Danchin
bioRxiv 362129; doi: https://doi.org/10.1101/362129

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