Identification of a volatile chemotype associated with resilience to water stress in domesticated varieties of cotton

BACKGROUND: Volatile organic compounds (VOCs) mediate plant responses to environmental stresses; yet, their chemotypic variation and drought responsiveness remain poorly characterized in domesticated crops. RESULTS: Here, we identify a previously undocumented binary chemotype structure in cultivated upland cotton (Gossypium hirsutum), defined by the mutually exclusive production of either bisabolene or guaiene sesquiterpenes. Across 24 genotypes grown under field conditions, 23 genotypes consistently produced one of these compounds (one genotype produced neither one nor the other compound), but never both, revealing a cryptic chemotypic polymorphism associated with different physiological responses to drought. While drought stress reduced leaf water content across all genotypes, the ones in the guaiene chemotype exhibited greater losses. Water limitation also reduced total monoterpene and sesquiterpene concentrations, with the bisabolene chemotype showing stronger declines despite higher constitutive levels. Chemotypes further diverged in their biosynthesis of key damage-induced green leaf volatiles (GLVs). While the guaiene chemotype reduced GLV biosynthetic capacity under prolonged drought, the bisabolene chemotype showed transient increases in GLVs and pathway-specific enzyme activity under short-term stress, suggesting differential physiological resilience. Notably, all genotypes in this study fell within the low γ-terpinene category previously described in wild cotton, indicating that this bisabolene/guaiene variation represents a novel axis of chemical diversity distinct from known wild chemotypes. CONCLUSIONS: These findings position chemotypic variation as a promising, non-destructive biomarker for drought differential responses. By linking chemotype to constitutive VOCs and water status, our work provides new tools for identifying stress-resilient cultivars and advances understanding of phytochemical strategies for crop management in a changing climate.