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The accumulation of the red carotenoid pigment lycopene in tomato ( Solanum lycopersicum ) fruit is achieved by increased carotenoid synthesis during ripening. The first committed step that determines the flux in the carotenoid pathway is the synthesis of phytoene catalyzed by phytoene synthase (PSY). Tomato has three  PSY  genes that are differentially expressed.  PSY1  is exclusively expressed in fruits, while  PSY2  mostly functions in green tissues. It has been established that PSY1 is mostly responsible for phytoene synthesis in fruits. Although PSY2 is found in the chromoplasts, it is inactive because loss-of-function mutations in  PSY1  in the locus  yellow flesh  ( r ) eliminate carotenoid biosynthesis in the fruit. Here we demonstrate that specific perturbations of carotenoid biosynthesis downstream to phytoene prior and during the transition from chloroplast to chromoplast cause the recovery of phytoene synthesis in  yellow flesh  ( r ) fruits without significant transcriptional changes of  PSY1  and  PSY2 . The recovery of carotenoid biosynthesis was abolished when the expression of  PSY2  was silenced, indicating that the perturbations of carotenoid biosynthesis reactivated the chloroplast-specific PSY2 in fruit chromoplasts. Furthermore, it is demonstrated that PSY2 can function in fruit chromoplasts under certain conditions, possibly due to alterations in the plastidial sub-organelle organization that affect its association with the carotenoid biosynthesis metabolon. This finding provides a plausible molecular explanation to the epistasis of the mutation  tangerine  in the gene  carotenoid isomerase  over  yellow flesh .

Perturbations in the Carotenoid Biosynthesis Pathway in Tomato Fruit Reactivate the Leaf-Specific Phytoene Synthase 2