Multiomics reveals postherbivory tea leaves restructure endophytic microbiota to resist disease and boost saccharide metabolism to promote growth

Abstract

Abstract The induced capacity of plant growth-defense trade-offs under biotic stress is increasingly recognized. While many studies focus primarily on plants’ defense activation stage during insect attacks, limited attention has been given to poststress recovery. Herein, leaves from normal and postherbivory tea plants were collected during the compensation stage, and their microbiomes, metabolomes, and transcriptomes were used to dissect the mechanisms underlying growth-defense trade-offs. The results revealed that apart from altering the microbial community diversity, insect herbivory significantly enriched leaf-associated pathogens, particularly Alternaria spp. Network analysis and in-situ separation jointly revealed the role of Sphingomonas aquatilis in resisting pathogen invasion. Meanwhile, the restructured microbiota exhibited stronger network stability, indicating the enhancement of pathogen resistance among the endophytic community. Moreover, integrated transcriptomic and metabolomic analysis revealed that genes such as GSGT1, GolS4, and α-gal may regulate synthesis and degradation of growth-promoting and defense metabolites. The downregulated flavonoids were defense compounds against pathogens and the upregulated saccharides were plant growth-promoting compounds, which were verified in subsequent tests. Overall, tea plants compensate for reduced defense through restructuring of the endophytic microbiota, and prioritize growth over defense through metabolic resetting after insect herbivory. This study also revealed new biocontrol and growth-promoting resources for tea plants.