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Role of the acquisition of a type 3 secretion system in the emergence of novel pathogenic strains of Xanthomonas

Valérian Méline 1 Wesley Delage 2 Chrystelle Brin 3 Camille Li-Marchetti 4 Daniel Sochard 5 Matthieu Arlat 6 Céline Rousseau 4 Armelle Darrasse 4 Martial Briand 4 Guillaume Lebreton 7 Perrine Portier 8 Marion Fischer-Le Saux 4 Karine Durand Marie-Agnès Jacques 4 Etienne Belin 9 Tristan Boureau 10, *
* Auteur correspondant
1 IRHS - Institut de Recherche en Horticulture et Semences
2 GenScale - Scalable, Optimized and Parallel Algorithms for Genomics
Inria Rennes – Bretagne Atlantique , IRISA-D7 - GESTION DES DONNÉES ET DE LA CONNAISSANCE
3 DPT SPE - Département Santé des Plantes et Environnement
4 IRHS - Institut de Recherche en Horticulture et Semences
5 AGROCAMPUS OUEST
6 LIPM - Laboratoire des interactions plantes micro-organismes
7 Service de Chirurgie Thoracique et Cardiovasculaire [CHU Pitié-Salpêtrière]
8 LECA - Laboratoire d'Ecologie Alpine
9 LARIS - Laboratoire Angevin de Recherche en Ingénierie des Systèmes
10 UNAM - PRES Université Nantes Angers Le Mans
Abstract : Cases of emergence of novel plant-pathogenic strains are regularly reported that reduce the yields of crops and trees. However, the molecular mechanisms underlying such emergence are still poorly understood. The acquisition by environmental non-pathogenic strains of novel virulence genes by horizontal gene transfer has been suggested as a driver for the emergence of novel pathogenic strains. In this study, we tested such an hypothesis by transferring a plasmid encoding the type 3 secretion system (T3SS) and four associated type 3 secreted proteins (T3SPs) to the non-pathogenic strains of Xanthomonas CFBP 7698 and CFBP 7700, which lack genes encoding T3SS and any previously known T3SPs. The resulting strains were phenotyped on Nicotiana benthamiana using chlorophyll fluorescence imaging and image analysis. Wild-type, non-pathogenic strains induced a hypersensitive response (HR)-like necrosis, whereas strains complemented with T3SS and T3SPs suppressed this response. Such suppression depends on a functional T3SS. Amongst the T3SPs encoded on the plasmid, Hpa2, Hpa1 and, to a lesser extent, XopF1 collectively participate in suppression. Monitoring of the population sizes in planta showed that the sole acquisition of a functional T3SS by non-pathogenic strains impairs growth inside leaf tissues. These results provide functional evidence that the acquisition via horizontal gene transfer of a T3SS and four T3SPs by environmental non-pathogenic strains is not sufficient to make strains pathogenic. In the absence of a canonical effector, the sole acquisition of a T3SS seems to be counter-selective, and further acquisition of type 3 effectors is probably needed to allow the emergence of novel pathogenic strains.© 2018 BSPP and John Wiley & Sons Ltd.
Keywords : Xanthomonas type 3 secretion system Chlorophyll Fluorescence Imaging Emergence non-pathogenic strains
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https://hal.univ-angers.fr/hal-02510889
Contributeur : Marie-Françoise Gerard <>
Soumis le : mercredi 18 mars 2020 - 11:38:28
Dernière modification le : lundi 2 août 2021 - 15:42:03

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UNIV-ANGERS | LARIS | INRA | LECA | AGROCAMPUS-OUEST | UNAM | UNIV-RENNES1 | IRHS | INRIA | UNIV-SAVOIE | UNIV-RENNES | IRISA | CNRS | INRAE | CENTRALESUPELEC | UR1-UFR-ISTIC | INSA-RENNES | UGA | SORBONNE-UNIVERSITE | SU-TI | LARIS-ISISV

Citation

Valérian Méline, Wesley Delage, Chrystelle Brin, Camille Li-Marchetti, Daniel Sochard, et al.. Role of the acquisition of a type 3 secretion system in the emergence of novel pathogenic strains of Xanthomonas. Molecular Plant Pathology, Wiley, 2019, 20 (1), pp.33-50. ⟨10.1111/mpp.12737⟩. ⟨hal-02510889⟩

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