Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles
2020
Emile, Gluck-Thaler, | Cerruti, A. | Pérez-Quintero, Alvaro L. | Veronica, Roman-Reyna, | Vishnu, Madhavan, | Deepak, Shantharaj, | Marcus,, Merfa, | Taca, Vancheva, | Beckham, Gregg T | de La Fuente, Leonardo | Hitendra, Patel, | Sonti, Ramesh V. | Leach, Jan E., J. E. | Noël, Laurent D. | Slot, Jason C. | Jacobs, Jonathan M. | Gluck-Thaler, Emile | Cerutti, Aude | Perez-Quintero, Alvaro, L | Butchacas, Jules | Roman-Reyna, Verónica | Madhavan, Vishnu, Narayanan | Shantharaj, Deepak | Merfa, Marcus, V | Pesce, Céline | Jauneau, Alain, A. | Vancheva, Taca | Lang, Jillian, M | Allen, Caitilyn | Verdier, Valerie | Gagnevin, Lionel | Szurek, Boris | Beckham, Gregg, T | De, Leonardo | Fuente, La | Patel, Hitendra, Kumar | Sonti, Ramesh, V | Bragard, Claude | Leach, Jan, E | Noël, Laurent | Slot, Jason, C | Koebnik, Ralf | Jacobs, Jonathan, M | The Ohio State University [Columbus] (OSU) | University of Pennsylvania | Laboratoire des Interactions Plantes Microbes Environnement (LIPME) ; Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Colorado State University [Fort Collins] (CSU) | Council of Scientific and Industrial Research [India] (CSIR) | Auburn University (AU) | Université Catholique de Louvain = Catholic University of Louvain (UCL) | National Renewable Energy Laboratory (NREL) | Institut de biologie de l'ENS Paris (IBENS) ; Département de Biologie - ENS-PSL (IBENS) ; École normale supérieure - Paris (ENS-PSL) ; Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL) ; Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS) | HM CLAUSE [USA Canada] | Plateforme Imagerie [Castanet-Tolosan] (IFR 3450 - Pôle de Biotechnologie Végétale) ; Institut Fédératif de Recherche | Colorado State University [Pueblo] (CSUPueblo) | University of Wisconsin-Madison | UMR - Interactions Plantes Microorganismes Environnement (UMR IPME) ; Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD [Occitanie]) | Département Systèmes Biologiques (Cirad-BIOS) ; Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad) | NSF Postdoctoral Fellowship in Biology : 1306196 | U.S. Fulbright Scholar Award | Science and Engineering Research Board, Government of India : SB/52/JCB-12/2014 | European Cooperation in Science and Technology (COST) : CA16107 EuroXanth | United States Department of Energy (DOE) : DE-AC36-08GO28308 | United States Department of Energy (DOE) | USDA NIFA Postdoctoral Fellowship : 2017-67012-26116 | COST SUSTAIN travel grant | National Science Foundation (NSF) : DEB-1638999 | Fonds de Recherche du Quebec-Nature et Technologies Doctoral Research Scholarship | University Grants Commission, India | Department of Science & Technology (India) | French Ministry of National Education and Research | USDA NIFA through NSF/NIFA Plant Biotic Interactions Program : 2018-67013-28490 | ANR-18-CE20-0020,NEPHRON,Analyse génétique et moléculaire de l'immunité de l'hydathode et du système vasculaire(2018) | ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010)
International audience
Show more [+] Less [-]English. Vascular plant pathogens travel long distances through host veins, leading to life-threatening, systemic infections. In contrast, nonvascular pathogens remain restricted to infection sites, triggering localized symptom development. The contrasting features of vascular and nonvascular diseases suggest distinct etiologies, but the basis for each remains unclear. Here, we show that the hydrolase CbsA acts as a phenotypic switch between vascular and nonvascular plant pathogenesis. cbsA was enriched in genomes of vascular phytopathogenic bacteria in the family Xanthomonadaceae and absent in most nonvascular species. CbsA expression allowed nonvascular Xanthomonas to cause vascular blight, while cbsA mutagenesis resulted in reduction of vascular or enhanced nonvascular symptom development. Phylogenetic hypothesis testing further revealed that cbsA was lost in multiple nonvascular lineages and more recently gained by some vascular subgroups, suggesting that vascular pathogenesis is ancestral. Our results overall demonstrate how the gain and loss of single loci can facilitate the evolution of complex ecological traits.
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