Signaling pathways mediated by jasmonic acid, ethylene, and IAA jointly regulate tea plant defense against hemibiotrophic fungal pathogens

Abstract

The tea plant, Camellia sinensis (L.) O. Kuntze, a perennial woody crop rich in secondary metabolites, faces severe threats from tea anthracnose (Colletotrichum camelliae). Although omics profiling and microarray analyses have described the tea plant’s responses to its causative pathogen infection, the mechanism underlying its induced immunity remains largely unknown. Here, we demonstrate that C. camelliae infection triggers both local and systemic resistance in tea plants, as evidenced by the curtailed local lesion expansion following foliar spore suspension pretreatment for 24 h, and the 1.2-fold suppression of lesions on leaves adjacent to a site inoculated for 48 h. Furthermore, C. camelliae infection activated jasmonic acid (JA)-, ethylene-, along with indole acetic acid (IAA)-mediated signaling pathways, promoting the accumulation of secondary metabolites, including isoschaftoside, isoquercitrin, cosmosiin, isovitexin, and feruloyl putrescine. Then, the bioassay using potato dextrose agar medium supplemented with these compounds confirmed their ability to suppress C. camelliae colony expansion in both time- and concentration-dependent manners: four compounds (isoquercitrin, cosmosiin, isovitexin, and isoschaftoside) exhibited strong negative correlations between concentration and colony diameter at 3 and 6 days (r ≤ –0.87, P < 0.001), while feruloyl putrescine showed a moderate correlation (r ≤ –0.51, P = 0.05–0.052), directly linking them to anti-anthracnose efficacy. Additionally, the exogenous application of the ethylene precursor 1-aminocyclopropane1-carboxylic acid, JA, and IAA significantly induced the accumulation of some of these anti-anthracnose metabolites in tea plants, which, in turn, enhanced the immunity of tea plants to C. camelliae. Therefore, this study not only highlights the critical role of a multi-hormone regulatory network in tea plant resistance to anthracnose, but also identifies the JA, IAA, and ET signaling pathways, along with five key metabolites, as promising targets for breeding resistant cultivars or developing plant immunity elicitors.