Light and Carbohydrate Signaling Genes Co-Regulate Carotenoid Accumulation in the Endocarp of Cucumber Fruit Under Photoperiodic Treatment as Revealed by Transcriptomic Analysis

The accumulation of carotenoids in edible plant organs is a key nutritional quality trait in many horticultural crops. Although the structural genes that encode the biosynthetic enzymes are well characterized, little is known regarding photoperiod-mediated carotenoid accumulation in the fruit of some horticultural crop species. An orange-fleshed Xishuangbanna (XIS) cucumber contains abundant β-carotene but it is short-photoperiod dependent. Moreover, the underlying molecular regulatory mechanism of the photoperiodic effect on the carotenoid accumulation in the endocarp XIS cucumber fruit remains largely unexplored. We performed physiological and RNA-seq analysis using two cucumber genotypes SWCC8 (XIS-orange-fleshed) and CC3 (White-fleshed), established under two photoperiod conditions (8L/16D vs 12L/12D) at four fruit developmental stages. Results show that day-neutral treatments significantly increased fruit β-carotene content by 42.1% compared to SD in XIS at 40 DAP with no significant changes in CC3. Sugar levels increased under day-neutral and decreased in short day durations. GO and KEGG analysis revealed that the predominantly expressed genes were mainly associated with the carbohydrate, circadian rhythm, carotenoid biosynthesis, plant hormone signaling, and photosynthesis. Day-neutral condition elevated expression of key carotenoid biosynthesis genes PSY1, PDS, ZDS1, LYCb, and CHY1 during later stages between 30 to 40 days of fruit development, which was consistent with β-carotene accumulation in XIS. Compared to XIS, CC3 showed expression of DEGs related to carotenoid cleavage and oxidative stresses. This could explain reduced β-carotene in CC3 and genotypic responses to photoperiod. Further analysis of WGCNA revealed that carbohydrate related genes (pentose-phosphatase synthase, β-glucosidase, and trehalose-6-phosphatase) and photoperiod signaling genes (LHY, APRR7/5, FKF1, PIF3, COP1, GIGANTEA, and CK2) co-express with the carotenoid biosynthetic genes, thus suggesting a cross-talk between carbohydrates and light related genes to induce β-carotene accumulation. Therefore, a mechanism of photoperiod-mediated carotenoid accumulation is envisaged involving synergistic interaction between light and carbohydrate-related genes. The results highlighted herein provide a framework for future gene mining for functional analysis and molecular breeding of carotenoid accumulation in plants.