title: Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi.
abstract: The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation. Here, we compare the genomes of a beneficial root endophyte, Colletotrichum tofieldiae and its pathogenic relative C. incanum, and examine the transcriptomes of both fungi and their plant host Arabidopsis during phosphate starvation. Although the two species diverged only 8.8 million years ago and have similar gene arsenals, we identify genomic signatures indicative of an evolutionary transition from pathogenic to beneficial lifestyles, including a narrowed repertoire of secreted effector proteins, expanded families of chitin-binding and secondary metabolism-related proteins, and limited activation of pathogenicity-related genes in planta. We show that beneficial responses are prioritized in C. tofieldiae-colonized roots under phosphate-deficient conditions, whereas defense responses are activated under phosphate-sufficient conditions. These immune responses are retained in phosphate-starved roots colonized by pathogenic C. incanum, illustrating the ability of plants to maximize survival in response to conflicting stresses.
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Stéphane
authors.initials: S
authors.lastname: Hacquard
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Barbara
authors.initials: B
authors.lastname: Kracher
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Kei
authors.initials: K
authors.lastname: Hiruma
authors.affiliation: German Center for Infection Research (DZIF), Partner Site Hannover-Braunschweig, 38124 Braunschweig, Germany.|Computational Biology of Infection Research, Helmholtz Center for Infection Research, 38124 Braunschweig, Germany.|Max-von-Pettenkofer Institute, LMU Munich, German Center for Infection Research (DZIF), Partner Site LMU Munich, 80336 Munich, Germany.
authors.forename: Philipp C
authors.initials: PC
authors.lastname: Münch
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.|Department of Algorithmic Bioinformatics, Heinrich Heine University Duesseldorf, 40225 Duesseldorf, Germany.|Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Ruben
authors.initials: R
authors.lastname: Garrido-Oter
authors.affiliation: Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Departamento de Microbiología y Genética, Universidad de Salamanca, 37185 Villamayor, Spain.
authors.forename: Michael R
authors.identifier: 0000-0002-7225-7003
authors.initials: MR
authors.lastname: Thon
authors.affiliation: Computational Biology of Infection Research, Helmholtz Center for Infection Research, 38124 Braunschweig, Germany.|Department of Algorithmic Bioinformatics, Heinrich Heine University Duesseldorf, 40225 Duesseldorf, Germany.
authors.forename: Aaron
authors.initials: A
authors.lastname: Weimann
authors.affiliation: CBS-KNAW Fungal Biodiversity Centre, 3584 CT Utrecht, The Netherlands.
authors.forename: Ulrike
authors.initials: U
authors.lastname: Damm
authors.affiliation: UMR BIOGER, INRA, AgroParisTech, Université Paris-Saclay, 78850 Thiverval-Grignon, France.
authors.forename: Jean-Félix
authors.initials: JF
authors.lastname: Dallery
authors.affiliation: CNRS UMR 7257, Aix-Marseille University, 13288 Marseille, France.|INRA, USC 1408 AFMB, 13288 Marseille, France.
authors.forename: Matthieu
authors.initials: M
authors.lastname: Hainaut
authors.affiliation: CNRS UMR 7257, Aix-Marseille University, 13288 Marseille, France.|INRA, USC 1408 AFMB, 13288 Marseille, France.|Department of Biological Sciences, King Abdulaziz University, 21589 Jeddah, Saudi Arabia.
authors.forename: Bernard
authors.initials: B
authors.lastname: Henrissat
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, 91405 Orsay, France.|Laboratoire de Recherche en Informatique, CNRS, Université Paris-Sud, 91405 Orsay, France.
authors.forename: Olivier
authors.initials: O
authors.lastname: Lespinet
authors.affiliation: Centro de Biotecnología y Genómica de Plantas (UPM-INIA) and E.T.S.I. Agrónomos, Universidad Politécnica de Madrid Campus de Montegancedo, 28223 Madrid, Spain.
authors.forename: Soledad
authors.initials: S
authors.lastname: Sacristán
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Emiel
authors.initials: E
authors.lastname: Ver Loren van Themaat
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.|Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Eric
authors.initials: E
authors.lastname: Kemen
authors.affiliation: Computational Biology of Infection Research, Helmholtz Center for Infection Research, 38124 Braunschweig, Germany.|Department of Algorithmic Bioinformatics, Heinrich Heine University Duesseldorf, 40225 Duesseldorf, Germany.|Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Alice C
authors.initials: AC
authors.lastname: McHardy
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.|Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
authors.forename: Paul
authors.initials: P
authors.lastname: Schulze-Lefert
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.|UMR BIOGER, INRA, AgroParisTech, Université Paris-Saclay, 78850 Thiverval-Grignon, France.
authors.forename: Richard J
authors.initials: RJ
authors.lastname: O'Connell
mesh_terms: D017360:Arabidopsis / Q000276:immunology / Q000378:metabolism*; D002686:Chitin / Q000378:metabolism; D020231:Colletotrichum / Q000235:genetics / Q000378:metabolism*; D060026:Endophytes / Q000235:genetics / Q000378:metabolism*; D016681:Genome, Fungal / Q000235:genetics; D010710:Phosphates / Q000172:deficiency*; D018517:Plant Roots / Q000378:metabolism*; D013217:Starvation; D013559:Symbiosis / Q000276:immunology / Q000502:physiology
chemical_list: D010710:Phosphates; D002686:Chitin