Phytoene synthases 1 modulates tomato fruit quality through influencing the metabolic flux between carotenoid and flavonoid pathways

The deterioration in fruit quality of commercial tomatoes is a major concern of modern tomato breeding. However, the metabolism and genetics of fruit quality are poorly understood. Here, we performed transgenic and molecular biology experiments to reveal that tomato phytoene synthase 1 (SlPSY1) is responsible for the accumulation of an important flavor chemical, 6-methyl-5-hepten-2-one (MHO). To dissect the function of SlPSY1 in regulating fruit quality, we generated and analyzed a dataset encompassing over 2 000 compounds detected by GC-MS and LC-MS/MS along with transcriptomic data. The combined results illustrated that SlPSY1 deficiency imparts novel flavor to yellow tomatoes with 236 volatiles significantly changed and improves fruit firmness, possibly due to accumulation of seven cutins. Further analysis indicated SlPSY1 is essential for carotenoid-derived metabolite biosynthesis by catalyzing prephytoene-PP (PPPP) to 15-cis-phytoene. Notably, we showed that SlPSY1 can influence the metabolic flux between carotenoid and flavonoid pathways, and this metabolic flux was confirmed by silencing SlCHS1. Our study provided insights into the multiple effects of SlPSY1 on tomato fruit metabolome and highlights the potential to produce high-quality fruit by rational design of SlPSY1 expression.