Bacterial host adaptation through sequence and structural variations of a single type III effector gene
Emmanuelle Lauber,
Manuel González-Fuente,
Maxime Escouboué,
Céline Vicédo,
Julien S. Luneau,
Cécile Pouzet,
Alain Jauneau,
Carine Gris,
Zhi-Min Zhang,
Carole Pichereaux,
Sébastien Carrère,
Laurent Deslandes,
Laurent D. Noël
Affiliations
Emmanuelle Lauber
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France
Manuel González-Fuente
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France
Maxime Escouboué
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France
Céline Vicédo
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France
Julien S. Luneau
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France
Cécile Pouzet
TRI-FRAIB Imaging Platform Facilities, FRAIB, Université de Toulouse, CNRS, UPS, 31320 Castanet-Tolosan, France
Alain Jauneau
TRI-FRAIB Imaging Platform Facilities, FRAIB, Université de Toulouse, CNRS, UPS, 31320 Castanet-Tolosan, France
Carine Gris
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France
Zhi-Min Zhang
International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), College of Pharmacy, Jinan University, Guangzhou 510632, China
Carole Pichereaux
Fédération de Recherche Agrobiosciences, Interactions et Biodiversité (FRAIB), Université de Toulouse, CNRS, Université de Toulouse III - Paul Sabatier (UT3), Auzeville-Tolosane, France; Institut de Pharmacologie et de Biologie Structurale (IPBS), Université de Toulouse, CNRS, Université de Toulouse III - Paul Sabatier (UT3), Toulouse, France; Infrastructure nationale de protéomique, ProFI, FR 2048, Toulouse, France
Sébastien Carrère
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France
Laurent Deslandes
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France; Corresponding author
Laurent D. Noël
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, F-31326 Castanet-Tolosan, France; Corresponding author
Summary: Molecular mechanisms underlying quantitative variations of pathogenicity remain elusive. Here, we identified the Xanthomonas campestris XopJ6 effector that triggers disease resistance in cauliflower and Arabidopsis thaliana. XopJ6 is a close homolog of the Ralstonia pseudosolanacearum PopP2 YopJ family acetyltransferase. XopJ6 is recognized by the RRS1-R/RPS4 NLR pair that integrates a WRKY decoy domain mimicking effector targets. We identified a XopJ6 natural variant carrying a single residue substitution in XopJ6 WRKY-binding site that disrupts interaction with WRKY proteins. This mutation allows XopJ6 to evade immune perception while retaining some XopJ6 virulence functions. Interestingly, xopJ6 resides in a Tn3-family transposon likely contributing to xopJ6 copy number variation (CNV). Using synthetic biology, we demonstrate that xopJ6 CNV tunes pathogen virulence on Arabidopsis through gene dosage-mediated modulation of xopJ6 expression. Together, our findings highlight how sequence and structural genetic variations restricted at a particular effector gene contribute to bacterial host adaptation.