Integrated volatile metabolome and transcriptome analysis unveils key biogenic volatile components enhancing aroma and stress tolerance in wheat

Biogenic volatile organic compounds (BVOCs) are critical for plant flavor quality, growth, and stress resistance, yet they remain poorly characterized in wheat. In this study, we performed volatile metabolome analysis on six wheat cultivars under normal and stress environments. A total of 476 BVOCs were detected, including esters, heterocyclic compounds, terpenoids, and other classes. Two-dimensional partial least squares-discriminant analysis (PLS-DA) effectively discriminated wheat samples from different environments, but failed to separate different cultivars. Notably, cultivars displayed distinct responses to stress. Certain cultivars exhibited low baseline BVOC levels but strong inducibility under stress, whereas others showed minimal BVOC variation. Terpenoids, particularly monoterpenes, were the most induced BVOC class across most cultivars, even in those stress insensitive cultivars. Transcriptomic profiling and co-expression network analysis identified gene modules correlated with total and specific BVOCs, which were enriched in genes involved in stress responses, sugar signaling, hormone signaling, and regulatory processes of gene expression. By integrating the expression profiles of core enzymes from four major BVOC biosynthetic pathways, we observed a decoupling between gene expression and BVOC variation. Further analysis focusing on monoterpene biosynthesis revealed that rate-limiting enzymes were up-regulated only in few cultivars, whereas the expression of genes involved in reducing power generation and carbon competition aligned with monoterpene variation. Functional assays demonstrated that among the co-upregulated BVOCs, 1,3-propanediol application promoted seedling growth under both normal and drought conditions, while 4-aminopyridine pretreatment enhanced potassium retention under salt stress. Collectively, our study provides novel insights into the mechanisms and functions underlying BVOC synthesis in wheat under stress.