Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato

Light signaling has long been reported to influence fruit biology, although the regulatory impact of fruit-localized photoreceptors on fruit development and metabolism remains unclear. Studies performed in phytochrome (PHY)-deficient tomato (Solanum lycopersicum) mutants suggest that SlPHYA, SlPHYB2, and to a lesser extent SlPHYB1 influence fruit development and ripening. By employing fruit-specific RNAi-mediated silencing of SlPHY genes, we demonstrated that fruit-localized SlPHYA and SlPHYB2 play contrasting roles in regulating plastid biogenesis and maturation in tomato. Our data revealed that fruit-localized SlPHYA, rather than SlPHYB1 or SlPHYB2, positively influences tomato plastid differentiation and division machinery via changes in both light and cytokinin signaling-related gene expression. Fruit-localized SlPHYA and SlPHYB2 were also shown to modulate sugar metabolism in early developing fruits via overlapping, yet distinct, mechanisms involving the co-ordinated transcriptional regulation of genes related to sink strength and starch biosynthesis. Fruit-specific SlPHY silencing also drastically altered the transcriptional profile of genes encoding light-repressor proteins and carotenoid-biosynthesis regulators, leading to reduced carotenoid biosynthesis during fruit ripening. Together, our data reveal the existence of an intricate PHY-hormonal interplay during fruit development and ripening, and provide conclusive evidence on the regulation of tomato quality by fruit-localized phytochromes.