Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi

Stéphane Hacquard, Barbara Kracher, Kei Hiruma, Philipp C. Münch, Ruben Garrido-Oter, Michael R. Thon, Aaron Weimann, Ulrike Damm, Jean-Félix Dallery, Matthieu Hainaut, Bernard Henrissat, Olivier Lespinet, Soledad Sacristán, Emiel Ver Loren van Themaat, Eric Kemen, Alice C. McHardy, Paul Schulze-Lefert () and Richard J. O’Connell ()
Additional contact information
Stéphane Hacquard: Max Planck Institute for Plant Breeding Research
Barbara Kracher: Max Planck Institute for Plant Breeding Research
Kei Hiruma: Max Planck Institute for Plant Breeding Research
Philipp C. Münch: German Center for Infection Research (DZIF), Partner Site Hannover-Braunschweig
Ruben Garrido-Oter: Max Planck Institute for Plant Breeding Research
Michael R. Thon: Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Universidad de Salamanca
Aaron Weimann: Computational Biology of Infection Research, Helmholtz Center for Infection Research
Ulrike Damm: CBS-KNAW Fungal Biodiversity Centre
Jean-Félix Dallery: UMR BIOGER, INRA, AgroParisTech, Université Paris-Saclay
Matthieu Hainaut: CNRS UMR 7257, Aix-Marseille University
Bernard Henrissat: CNRS UMR 7257, Aix-Marseille University
Olivier Lespinet: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud
Soledad Sacristán: Centro de Biotecnología y Genómica de Plantas (UPM-INIA) and E.T.S.I. Agrónomos, Universidad Politécnica de Madrid Campus de Montegancedo
Emiel Ver Loren van Themaat: Max Planck Institute for Plant Breeding Research
Eric Kemen: Max Planck Institute for Plant Breeding Research
Alice C. McHardy: Computational Biology of Infection Research, Helmholtz Center for Infection Research
Paul Schulze-Lefert: Max Planck Institute for Plant Breeding Research
Richard J. O’Connell: Max Planck Institute for Plant Breeding Research

Nature Communications, 2016, vol. 7, issue 1, 1-13

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms11362

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