Identification of a lipase gene with a role in tomato fruit short-chain fatty acid-derived flavor volatiles by genome-wide association.

Fatty acid-derived volatile organic compounds (FA-VOCs) make significant contributions to tomato (Solanum lycopersicum) fruit flavor and human preferences. Short-chain FA-VOCs (C5 and C6) are among the most abundant and important volatile compounds in tomato fruits. The precursors of these volatiles, linoleic acid (18:2) and linolenic acid (18:3), are derived from cleavage of glycerolipids. However, the initial step in synthesis of these FA-VOCs has not been established. A metabolite-based genome-wide association study combined with genetic mapping and functional analysis identified a gene encoding a novel class III lipase family member, Sl-LIP8, that is associated with accumulation of short-chain FA-VOCs in tomato fruit. In vitro assays indicated that Sl-LIP8 can cleave 18:2 and 18:3 acyl groups from glycerolipids. A CRISPR/Cas9 gene edited Sl-LIP8 mutant had much lower content of multiple fruit short-chain FA-VOCs, validating an important role for this enzyme in the pathway. Sl-LIP8 RNA abundance was correlated with FA-VOC content, consistent with transcriptional regulation of the first step in the pathway. Taken together, our work indicates that glycerolipid turnover by Sl-LIP8 is an important early step in the synthesis of multiple short-chain FA-VOCs.