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 ( SlYHB1 ^OE and SlYHB2 ^OE ). The impaired cuticle of SlYHB1/B2 ^OE 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.