Specific sets of geranylgeranyl diphosphate synthases and phytoene synthases control the production of carotenoids...

Plant carotenoids are plastid-synthesized isoprenoids with roles as photoprotectants, pigments, and precursors of bioactive molecules such as the hormone abscisic acid (ABA). The first step of the carotenoid biosynthesis pathway is the production of phytoene from geranylgeranyl diphosphate (GGPP), catalyzed by phytoene synthase (PSY). GGPP produced by plastidial GGPP synthases (GGPPS) is channeled to the carotenoid pathway by direct interaction of GGPPS and PSY enzymes. Three plastid-localized GGPPS isoforms (referred to as SlG1-3) and three PSY enzymes (PSY1-3) are present in tomato (Solanum lycopersicum). Our previous work showed that SlG1 and PSY3 function together in the roots, whereas the rest of the isoforms are required in aerial tissues. Here we generated and analyzed combinations of double mutants lacking PSY1 or PSY2 and SlG2 or SlG3 to investigate the contribution of specific GGPPS and PSY pairs to the production of carotenoids and ABA in different tissues of the tomato plant. Despite that the loss of individual enzymes was found to trigger compensatory mechanisms that complicate interpretation of the results, the results confirm a major role for SlG3 in providing GGPP to PSY2 for housekeeping carotenoid biosynthesis in leaves, whereas SlG2 and PSY1 become most relevant when a more active production is required in flowers and breaker fruits, i.e., at the onset of ripening. We could also confirm that ABA production in the fruit pericarp is more dependent on PSY1 activity than on total carotenoid levels and that fruit size correlates with ABA levels accumulated in ripe rather than breaker fruits.