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

• DOI: 10.1038/ncomms11362
• Publication Date: 2016-05-06T09:58:40Z
• Authors: 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 v...; Eric Kemen; Alice C. McHardy; Paul Schulze-Lefert; Richard J. O’Connell
• Keywords: roots; 570; Colletotrichum tofieldiae; Arabidopsis thaliana; plant innate immunity; [SDV]Life Sciences [q-bio]; Biología; Science; Arabidopsis; Chitin; Plant Roots; Article; Phosphates; 03 medical and health sciences; Colletotrichum; Endophytes; Colletotrichum tofieldiae ;Colletotrichum incanum;Arabidopsis thaliana;endophyte ;roots ;plant innate immunity ;genome;transcriptome;differential gene expression;symbiosis; Colletotrichum incanum; differential gene expression; Symbiosis; genome; 2. Zero hunger; 0303 health sciences; Agricultura; Q; 15. Life on land; symbiosis; [SDV] Life Sciences [q-bio]; Starvation; Genome, Fungal; endophyte; transcriptome

AbstractThe 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.