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.
Highlights
The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation
We sequenced the genome of the plant growth-promoting fungus C. tofieldiae (Ct) isolate 0861, a root endophyte isolated from natural populations of A. thaliana in Spain[8,10], and those of four other Ct isolates isolated from diverse dicot and monocot hosts in Europe (Supplementary Note 1)
Our phylogenetic analysis suggests that evolution from pathogenic ancestors towards the beneficial endophytic lifestyle in Ct is a recent adaptation in Colletotrichum fungi
Summary
The sessile nature of plants forced them to evolve mechanisms to prioritize their responses to simultaneous stresses, including colonization by microbes or nutrient starvation. Colonization of A. thaliana roots by the closely related pathogenic species C. incanum (Ci), which attacks members of the Brassicaceae, Fabaceae and Solanaceae, severely inhibited Arabidopsis growth and mediated only low levels of 33P translocation into shoots[8]. These findings raise the possibility that in low-phosphate soils, root colonization by the Ct endophyte compensates for the absence of key genetic components required for mycorrhizal symbiosis in the Brassicaceae lineage, which is otherwise conserved in B80–90% of terrestrial plants[9]. Our findings shed light on the ability of plants to maximize survival by prioritizing their responses to simultaneous biotic and abiotic stresses
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