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Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles

Authors :
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.
Noël, Laurent D.
Slot, Jason C.
Jacobs, Jonathan M.
Gluck-Thaler, Emile
Cerutti, Aude
Perez-Quintero, Alvaro
Butchacas, Jules
Roman-Reyna, Verónica
Madhavan, Vishnu
Shantharaj, Deepak
Merfa, Marcus
Pesce, Céline
Jauneau, Alain
Vancheva, Taca
Lang, Jillian
Allen, Caitilyn
Verdier, Valerie
Gagnevin, Lionel
Szurek, Boris
Beckham, Gregg
De, Leonardo
Fuente, La
Patel, Hitendra
Sonti, Ramesh
Bragard, Claude
Leach, Jan
Noël, Laurent
Slot, Jason
Koebnik, Ralf
Jacobs, Jonathan
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 Paris
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 [France-Sud])
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)
University of Pennsylvania [Philadelphia]
Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Département de Biologie - ENS Paris
École normale supérieure - Paris (ENS Paris)
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 Paris)
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 de biologie de l'ENS Paris (UMR 8197/1024) (IBENS)
Source :
Science Advances, Science Advances, 2020, 6 (46), ⟨10.1126/sciadv.abc4516⟩, Science Advances, American Association for the Advancement of Science (AAAS), 2020, 6 (46), ⟨10.1126/sciadv.abc4516⟩
Publication Year :
2020
Publisher :
HAL CCSD, 2020.

Abstract

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. evolution of complex ecological traits.

Details

Language :
English
ISSN :
23752548
Database :
OpenAIRE
Journal :
Science Advances, Science Advances, 2020, 6 (46), ⟨10.1126/sciadv.abc4516⟩, Science Advances, American Association for the Advancement of Science (AAAS), 2020, 6 (46), ⟨10.1126/sciadv.abc4516⟩
Accession number :
edsair.doi.dedup.....5bd48b6ac064eb4612891cdadc3a9c6b
Full Text :
https://doi.org/10.1126/sciadv.abc4516⟩