Light-induced variation in phenolic compounds in Cabernet Sauvignon grapes (Vitis vinifera L.) involves extensive transcriptome reprogramming of biosynthetic enzymes, transcription factors, and phytohormonal regulators

Light environments have long been known to influence grape (Vitis vinifera L.) berry development and biosynthesis of phenolic compounds, and ultimately affect wine quality. Here, the accumulation and compositional changes of hydroxycinnamic acids (HCAs) and flavonoids, as well as global gene expression were analyzed in Cabernet Sauvignon grape berries under sunlight exposure treatments at different phenological stages. Sunlight exposure did not consistently affect the accumulation of berry skin flavan-3-ol or anthocyanin among different seasons due to climatic variations, but increased HCA content significantly at véraison and harvest, and enhanced flavonol accumulation dramatically with its timing and severity degree trend. As in sunlight exposed berries, a highly significant correlation was observed between the expression of genes coding phenylalanine ammonia-lyase, 4-coumarate: CoA ligase, flavanone 3-hydroxylase and flavonol synthase family members and corresponding metabolite accumulation in the phenolic biosynthesis pathway, which may positively or negatively be regulated by MYB, bHLH, WRKY, AP2/EREBP, C2C2, NAC, and C2H2 transcription factors (TFs). Furthermore, some candidate genes required for auxin, ethylene and abscisic acid signal transductions were also identified which are probably involved in berry development and flavonoid biosynthesis in response to enhanced sunlight irradiation. Taken together, this study provides a valuable overview of the light-induced phenolic metabolism and transcriptome changes, especially the dynamic responses of TFs and signaling components of phytohormones, and contributes to the further understanding of sunlight-responsive phenolic biosynthesis regulation in grape berries. In three consecutive years (2011-2013), eight fruit-zone light exposure levels were established in the vines through artificial leaf removal, half leaf removal, or leaf moving: leaf removal at berry pepper-corn size (LR-PS); leaf removal at véraison (LR-V); leaf removal after véraison (LR-AV); half leaf removal at véraison (HLR-V); half leaf removal after véraison (HLR-AV); leaf moving at véraison (LM-V); leaf moving after véraison (LM-AV); and non-treated control (C). Leaf removal and half leaf removal treatments were carried out by removing the first one to six basal leaves from the main shoots with clusters and three basal leaves from the first, third, and fifth of each shoot with clusters, respectively. For leaf moving treatment, the first one to six basal leaves of each shoot with clusters were moved aside by the use of nylon zipties, in order to increase the sunlight exposure of grape clusters without affecting the photosynthetic carbon assimilation to the fruit. Each treatment was arranged in a completely randomized experimental design with three biological replicates. In each biological replicate, treatment was applied to 15 vines randomly selected from the vineyard's south and north sites. Berries from each treatment and control group were sampled at the following developmental time points: 3 weeks after flowering (waf) (berry pepper-corn size; E-L 29), five waf (berry pea-size, E-L 31), seven waf (berry still hard and green, E-L 33), early-véraison (berries begin to color, E-L 35), mid-ripening stage (berries with intermediate Brix values, E-L 36), end of véraison (berries not quite ripe, E-L 37) and complete ripening stage (E-L 38). Based on biochemical parameters and metabolite profiles, we selected the berries of three developmental stages (E-L 36, 37, and 38) from the LR-V and LM-V treatments and the control group during the 2012 growing season to conduct the transcriptome profiling analysis. Please note that GSM4762225-GSM4762233 are re-analysis of GSM3727972-GSM3727980 in GSE129916, respectively, and are the duplicated sample records for the convenient retrieval of the complete raw data from SRA.