Integrated transcriptome and metabolome analysis reveal a reprogramming of phenylpropanoid pathway and antioxidant...

Anthracnose, caused by Colletotrichum gloeosporioides (Cog), severely constrains the Cymbidium ensifolium industry. To investigate the molecular underpinnings of resistance and the host-pathogen interaction strategies between C. ensifolium and Cog, we employed transcriptomics and metabolomics to compare the post-infection responses of the Cog-resistant (RV) and Cog-susceptible (SV) C. ensifolium varieties. Our integrated analysis reveals that resistance to Cog in C. ensifolium is partially mediated by the targeted accumulation of phenylpropane pathway metabolites, especially those involved in flavone and flavonol biosynthesis. Metabolites including rutin, lonicerin, nicotiflorin, apiin, and coniferin exhibited highly significant accumulation in the RV. The massive accumulation of various flavonoids in the SV was consistent with the gene expression trends in the phenylpropanoid pathway, a pattern indicative of an antioxidant stress response driven by stress reprogramming. A similar phenomenon was also observed in the core reactive oxygen species (ROS) scavenging pathway, glutathione metabolism. This ultimately results in two distinct outcomes: a potent, antifungal defense reprogramming in the RV versus an antioxidant-focused stress reprogramming in the SV. The observed trade-offs between antifungal and antioxidant activities in these varieties provide novel insights into the multilevel regulatory networks governing plant-pathogen interactions. Our study illuminates this sophisticated defense strategy of C. ensifolium against Cog, identifying core metabolites and pathways that now serve as a guide for targeted resistance breeding programs.