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.