Jasmonic acid and ethylene are the key signaling molecules ofE. sibirica -mediated induced systemic resistance
Jasmonic acid has been reported to be a fundamental signaling molecule of ISR, which emerged as a crucial mechanism in priming the whole plant body for enhanced defense against a broad range of pathogens by plant growth-promoting microorganisms (Pieterse et al., 2014), such as arbuscular mycorrhizal fungi (Nair et al., 2015) and Trichoderma(Ji et al., 2021). In addition, ET can also cooperate with JA to trigger ISR regulated by some Trichoderma species (Shoresh et al., 2005; Yuan et al., 2019). As for endophytes, manyEpichloë species can promote the growth of the host grasses and improve the disease resistance of hosts (Bastías et al., 2021; Pérez et al., 2020), whether it generates ISR or not remains unclear. Guo et al. (2019) found thatEpichloë festucae var. lolli infection improved the disease resistance of L. perenne while had a null effect on JA content. In another study, E. gansuensis enhanced the resistance of A. inebrians to pathogens but significantly decreased JA content in hosts (Kou et al., 2021). As for ET, there is currently no available research on the influence of endophytic infection on the ET content of the host grasses.
In this study, the result of integrated transcriptome and metabolomics KEGG enriched analysis unveiled that plant hormone signal transduction was significantly enriched after pathogen inoculation, suggesting that plant hormone signaling might be a critical pathway for enhancing the host’s disease resistance by endophytes. Moreover, endophytes significantly increased JA and ET contents and upregulated gene expression levels in the JA/ET signaling pathway. Exogenous hormone treatment further corroborated the positive effect of JA/ET on A. sibiricum resistance to C. lunata . Thus, we hypothesize that endophytes activate the ISR of the host by inducing JA accumulation before pathogen inoculation and promote JA and ET synthesis after pathogen inoculation.
Akin to SA, Pip is also a key signal molecule of SAR in plants (Klessig et al., 2018). Herein, endophytes had no significant effect on SA content, although they promoted Pip accumulation after pathogen inoculation. Pip was reported to be a critical regulator of SAR to biotrophic pathogens (Chen et al., 2018). Here, exogenous chemicals treatment did not verify the positive effect of Pip on necrotrophicC. lunata . In previous research, endophytes could also enhance the resistance of A. sibiricum to biotrophs but had no significant effect on SA content (Shi et al., 2020), which suggests that endophytes may improve the resistance of the host to biotrophs via the Pip signaling pathway.
Endophyte induced remodeling of genes expression and metabolites accumulation inphenylpropanoid biosynthesis pathway in the host
Plants can resist the invasion of pathologic microorganisms by synthesizing phenolic compounds (Balasundram et al., 2006). Pańka et al. (2013a, 2013b) found that endophytes might enhance disease resistance by increasing the total phenolic content in grasses, but changes in phenolic metabolites were not evaluated. In this research, endophytes activated the transcription of PTAL and 4CL genes involved in the synthesis of phenolic substances and promoted the accumulation of ferulic acid, p-coumaroylagmatine, and feruloylputrescine in the tyrosine metabolism pathway in the host. Ferulic acid (Reem et al ., 2016), p-coumaroylagmatine (Ube et al., 2017), and feruloylputrescine (Valette et al., 2020) can be synthesized in large quantities in response to plant diseases and have significant antimicrobial activities. Therefore, our results suggest that endophytes may enhance the host’s disease resistance by promoting the accumulation of ferulic acid, p-coumaroylagmatine, and feruloylputrescine through the l-tyrosine metabolism pathway.