Multi-omics integration to explore the molecular insight into the volatile organic compounds in watermelon

A range of volatile organic compounds played an important role in the formation of watermelon fruit aroma, while due to the low content and difficulty in detection, it is often neglected in watermelon breeding programs, resulting in a decline in fruit flavor. VOCs in the flesh of 194 watermelon accessions and seven cultivars at four developmental stages were determined by SPME-GC-MS. Ten metabolites with significant differences in the natural population and positive accumulation during fruit development are considered to be the key metabolite related to watermelon fruit aroma. And the link between metabolite and, flesh color and sugar content by correlation analysis was established. The results of the genome-wide association study showed that (5E)-6,10-dimethylundeca-5,9-dien-2-one, and 1-(4-methylphenyl) ethanone were colocalized with watermelon flesh color on chromosome 4, which may be regulated by LCYB and CCD. (E)-4-(2,6,6-trimethylcyclohexen-1-yl)but-3-en-2-one is the VOC produced by the cleavage of carotenoids, which has a positive correlation with the sugar content of the fruit, and the candidate gene Cla97C05G092490 on chromosome 5 may interact with PSY to influence the accumulation of this metabolite. In addition, Cla97C02G049790 (enol reductase), Cla97C03G051490 (omega-3 fatty acid desaturase gene), LOX, and ADH may play important roles in the synthesis of fatty acids and their derived VOCs. Taken together, our findings provide molecular insights into the accumulation and natural variation of VOCs in watermelon, and give data support for breeding watermelon cultivars with better flavor.