Grape color variation involves genetic and micro-environmental changes that alter berry phenolic and aromatic composition

Black- and white-berried grapevine cultivars are distinguished by their ability to accumulate anthocyanins in the berry skin. To assess possible side effects of color variation in berry development and composition in a near-isogenic background, we compared white-berried somatic variants (WV) to their black-berried ancestors in 'Garnacha' and 'Tempranillo' cultivars. Absence of anthocyanins correlated with lower berry temperature during daytime in WV. At the transcriptome level, besides genes related to anthocyanin accumulation, transcripts encoding enzymes involved in flavonoid backbone biosynthesis and modification were downregulated from veraison in WV skin. Genes mapping to hemizygous genome regions in WV were also downregulated irrespective of berry tissue or developmental stage. Light-responsive genes including flavonol and monoterpenoid biosynthesis genes were upregulated in WV from veraison. In agreement, flavonol partitioning was altered and tri-hydroxylated forms were practically absent in WV, whereas higher levels of specific volatile monoterpenoids and their soluble precursors were detected in WV pericarp. Amino acid precursors of phenolic compounds tended to be higher in WV pericarp. Collectively, greater differences were observed in 'Tempranillo' than in 'Garnacha', revealing effects of genetic background. These results indicate that the grape color locus directly controls the metabolism of colorless flavonoids, whereas additional alterations in grape quality compounds are established in a cultivar-dependent manner in response to alteration of the berry microclimate caused by the absence of anthocyanins.