Multi-omics integration reveals an α-linolenic acid-jasmonic acid regulatory network underlying fiber heterosis in cotton hybrid breeding

Heterosis is a crucial genetic phenomenon for crop breeding, but its molecular mechanisms in cotton remain unclear. Gossypium hirsutum cv. Xinluzao 67 (XLZ67), a superior hybrid derived from 44 to 32 and 68–38, exhibits prominent heterosis in fiber yield and quality. To dissect its heterotic basis, we integrated transcriptomic and metabolomic analyses of fiber at 0, 5, 10, and 25 days post-anthesis (DPA) from XLZ67 and its parents. 77,341 expressed genes and 2052 annotated metabolites were identified. Stage-specific clustering of transcriptomic and metabolomic data revealed coordinated gene-metabolite regulation during fiber development. Among these, 3.22%–5.50% of genes and 3.15%–5.82% of metabolites showed non-additive expression/accumulation patterns, which were enriched in lipid metabolism pathways (α-linolenic acid, linoleic acid, etc.). Notably, α-linolenic acid metabolism was consistently active across all stages. Key intermediates (phosphatidylcholine, stearidonic acid, 13(S)-HpOTrE) and jasmonic acid (JA) biosynthetic genes were upregulated in XLZ67, especially at 5–10 DPA. Stage-specific transcriptional and metabolic patterns during fiber development (differentiation at 0 DPA, elongation at 5–10 DPA, thickening at 25 DPA) revealed coordinated gene-metabolite regulation, with non-additively expressed genes and accumulated metabolites serving as key contributors to heterosis. We propose that parental genetic complementation activates α-linolenic acid metabolism, enhancing JA biosynthesis to promote fiber cell elongation. This study uncovers a novel α-linolenic acid-JA regulatory axis underlying cotton heterosis, providing molecular markers for hybrid breeding. • Cotton hybrid XLZ67 overcomes the yield-fiber quality trade-off. • Integrated multi-omics identifies non-additive genes and non-additive metabolites. • A novel α-linolenic acid-jasmonic acid axis drives fiber heterosis, with key pathway components upregulated in XLZ67. • Parental genetic complementation activates α-linolenic acid metabolism, boosting JA biosynthesis to promote fiber elongation.