Changes in DNA methylation contribute to rapid adaptation in bacterial plant pathogen evolution

Gopalan-Nair Rekha, Coissac Aurore, Legrand Ludovic, Lopez-Roques Céline, Pecrix Yann, Vandecasteele Céline, Bouchez Olivier, Barlet Xavier, Lanois Anne, Givaudan Alain, Brillard Julien, Genin Stéphane, Guidot Alice. 2024. Changes in DNA methylation contribute to rapid adaptation in bacterial plant pathogen evolution. PLoS Biology, 22 (9):e3002792, 31 p.

https://doi.org/10.1371/journal.pbio.3002792

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Liste HCERES des revues (en SHS) : oui

Thème(s) HCERES des revues (en SHS) : Psychologie-éthologie-ergonomie

Résumé : Adaptation is usually explained by beneficial genetic mutations that are transmitted from parents to offspring and become fixed in the adapted population. However, genetic mutation analysis alone is not sufficient to fully explain the adaptive processes, and several studies report the existence of nongenetic (or epigenetic) inheritance that can enable adaptation to new environments. In the present work, we tested the hypothesis of the role of DNA methylation, a form of epigenetic modification, in adaptation of the plant pathogen Ralstonia pseudosolanacearum to the host during experimental evolution. Using SMRT-seq technology, we analyzed the methylomes of 31 experimentally evolved clones obtained after serial passages on 5 different plant species during 300 generations. Comparison with the methylome of the ancestral clone revealed a list of 50 differential methylated sites (DMSs) at the GTWWAC motif. Gene expression analysis of the 39 genes targeted by these DMSs revealed limited correlation between differential methylation and differential expression of the corresponding genes. Only 1 gene showed a correlation, the RSp0338 gene encoding the EpsR regulator protein. The MSRE-qPCR technology, used as an alternative approach for DNA methylation analysis, also found the 2 DMSs upstream RSp0338. Using site-directed mutagenesis, we demonstrated the contribution of these 2 DMSs in host adaptation. As these DMSs appeared very early in the experimental evolution, we hypothesize that such fast epigenetic changes can allow rapid adaptation to the plant stem environment. In addition, we found that the change in DNA methylation upstream RSp0338 remains stable at least for 100 generations outside the host and thus can contribute to long-term adaptation to the host plant. To our knowledge, this is the first study showing a direct link between bacterial epigenetic variation and adaptation to a new environment.

Mots-clés Agrovoc : Ralstonia solanacearum, méthylation, adn, expression des gènes, Solanum lycopersicum, génétique des populations, évolution, mutation, adaptation, phylogénie, pathologie végétale

Mots-clés libres : Ralstonia solanacearum species complex, Epigenetics, Genomics, Bacterial wilt

Classification Agris : F30 - Génétique et amélioration des plantes
H20 - Maladies des plantes

Champ stratégique Cirad : CTS 4 (2019-) - Santé des plantes, des animaux et des écosystèmes

Agences de financement européennes : European Commission, European Regional Development Fund

Agences de financement hors UE : Agence Nationale de la Recherche, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, France Génomique

Projets sur financement : (FRA) Rôle des modifications épigénétiques chez un pathogène de plante au cours de l'adaptation à l'hôte et des changements d'hôte, (FRA) Towards a Unified theory of biotic Interactions: the roLe of environmental, (FRA) France Génomique-INBS

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