Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity

During a compatible interaction, the sebacinoid root-associated fungi Piriformospora indica and Sebacina vermifera induce modification of root morphology and enhance shoot growth in Arabidopsis thaliana. The genomic traits common in these two fungi were investigated and compared with those of other root-associated fungi and saprotrophs. The transcriptional responses of the two sebacinoid fungi and of Arabidopsis roots to colonization at three different symbiotic stages were analyzed by custom-designed microarrays. We identified key genomic features characteristic of sebacinoid fungi, such as expansions for gene families involved in hydrolytic activities, carbohydrate-binding and protein-protein interaction. Additionally, we show that colonization of Arabidopsis correlates with the induction of salicylic acid catabolism and accumulation of jasmonate and glucosinolates (GSLs). Genes involved in root developmental processes were specifically induced by S.vermifera at later stages during interaction. Using different Arabidopsis indole-GSLs mutants and measurement of secondary metabolites, we demonstrate the importance of the indolic glucosinolate pathway in the growth restriction of P.indica and S.vermifera and we identify indole-phytoalexins and specifically indole-carboxylic acids derivatives as potential key players in the maintenance of a mutualistic interaction with root endophytes.