Epichloë endophytes can improve the resistance of host grasses to pathogenic fungi in grasslands. However, little is known about the mechanisms involved. We investigated the mechanisms underlying the effect of Epichloë sibirica on the resistance of Achnatherum sibiricum to Curvularia lunata by metabolomics approaches. The results demonstrated that before and after pathogen inoculation, 58 and 157 differential metabolites (DMs) were respectively induced by endophytes. Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses of DMs showed that amino acids and phenols were mostly accumulated by endophytic infection. Integrated transcriptome and metabolomics KEGG analysis revealed that plant hormone signal transduction was significantly enriched. After measurement, we found that endophytic infection increased jasmonic acid (JA) concentration before pathogen inoculation and increased ethylene (ET) and pipecolic acid concentration after pathogen inoculation. Exogenous phytohormones treatment verified that endophytes improved the disease resistance of A. sibiricum by promoting JA and ET accumulation. In phenylpropanoid synthetic pathway, the endophytes promoted the accumulation of ferulic acid, p-coumaroylagmatine, and feruloylputrescine which was related to resistance against plant disease. Overall, our research suggests that Epichloë endophytes presumably trigger induced systemic resistance of the hosts to pathogenic fungi via activating JA/ET signaling pathways and promoted antimicrobial phenol accumulation in hosts.

Epichloë endophytes can improve the resistance of host grasses to pathogenic fungi. However, little is known about the mechanisms involved. We studied the effect of Epichloë sibirica on the resistance of Achnatherum sibiricum to Curvularia lunata. Then, the global gene expression between endophyte-infected and endophyte-free leaves was compared. Finally, exogenous hormones were applied to verify the action mechanism of the endophyte. The endophyte improved pathogen resistance of host. Before pathogen inoculation, the endophyte had activated the host’s immunity by increasing jasmonic acid (JA) accumulation, and upregulating the expression of genes encoding pathogenesis-related proteins and EIN3/ERF1 transcription factors. After pathogen inoculation, the endophyte increased the accumulation of both JA and ethylene (ET), and amplified the gene response in the EIN3/ERF1 transduction pathway. Moreover, the endophyte altered the expression of genes encoding putative WRKY transcription factors and glutathione-S-transferase, which are related to disease resistance. Overall, this work first revealed that E. sibirica enhanced the resistance of A. sibiricum to C. lunata by inducing the response of EIN3/ERF1 transduction pathway regulated jointly by JA/ET. Before pathogen inoculation, the endophyte induced JA accumulation to improve constitutive resistance in the host. After pathogen inoculation, the endophyte enhanced the induced systemic resistance by promoting ET synthesis.