Shedding light on cuticle formation: phytochrome B and downstream signaling events controlling cuticle deposition in tomato fruits

The cuticle is a hydrophobic barrier limiting water loss and pathogen entry. Although light influences cuticle formation, the underlying mechanisms remain poorly understood, particularly in fruits. Here, we show that fruits from tomato (Solanum lycopersicum) plants grown under far-red-enriched light conditions displayed increased cuticle load due to the up-regulation of cutin and wax biosynthetic genes. Both tomato PHYB-encoding genes (SlPHYB1 and SlPHYB2) were implicated as negative regulators of fruit cuticle formation, as revealed by the thinner cuticles, reduced abundance of cutin monomers and cuticular waxes, and downregulation of cuticle-related genes detected in fruits from transgenic plants overexpressing constitutively active alleles of SlPHYB1/B2 (SlYHB1OE and SlYHB2OE). The impaired cuticle of SlYHB1/B2OE fruits resulted in increased susceptibility to Botrytis cinerea, despite their markedly enhanced flavonoid accumulation in the peel. PHYTOCHROME-INTERACTING FACTORs (SlPIF3, SlPIF4) and the B-box protein SlBBX28 were identified as downstream factors of SlPHYB1/B2-mediated regulation of cuticle deposition, synergistically activating the expression of cuticle-related genes. Additionally, SlPHYB1/B2 signaling also downregulated multiple central carbon metabolism-related genes in the fruit peel, likely reducing the pool of activated fatty acids (FAs) feeding into cutin and wax biosynthetic pathways. Together, our results uncover a novel regulatory layer of light signaling in fleshy fruits, revealing that, besides controlling fruit nutritional traits, the PHYB-PIF-BBX regulatory module also shapes the fruit cuticle formation.