Overlapping and specialized roles of tomato phytoene synthase isoforms PSY1 and PSY2 in carotenoid and ABA production

Carotenoids are plastidial isoprenoids required for photosynthesis and production of hormones such as abscisic acid (ABA) in all plants. In tomato (Solanum lycopersicum), carotenoids also provide color to flowers and ripe fruit. Phytoene synthase (PSY) catalyzes the first and main flux-controlling step of the carotenoid pathway. Three PSY isoforms are present in tomato, PSY1 to 3. Mutants have shown that PSY1 is the isoform providing carotenoids for fruit pigmentation but it is dispensable in photosynthetic tissues. No mutants are available for PSY2 or PSY3, but their expression profiles suggest a main role for PSY2 in leaves and PSY3 in roots. To further investigate isoform specialization with genetic tools, we created tomato edited lines defective in PSY1 and PSY2 in the MicroTom background. The albino phenotype of lines lacking both PSY1 and PSY2 confirmed that PSY3 does not contribute to carotenoid biosynthesis in shoot tissues. Our work further shows that carotenoid production in tomato shoots relies on both PSY1 and PSY2 but with different contributions in different tissues. PSY2 is the main isoform for carotenoid biosynthesis in leaf chloroplasts, but the supporting role of PSY1 is particularly important under high light. PSY2 also contributes to the production of carotenoids in flower petals and, to a lower extent, fruit chromoplasts. Most interestingly, our results demonstrate that fruit growth and ripening is controlled by ABA produced in the pericarp from PSY1-derived precursors whereas PSY2 provides precursors for ABA synthesis in seeds to control germination.