A Sense of Place: Transcriptomics Identifies Environmental Signatures in Cabernet Sauvignon Berry Skins in the Late Stages of Ripening.

Background: Grape berry ripening is influenced by climate, the main component of the “terroir” of a place. Light and temperature are major factors in the vineyard that affect berry development and fruit metabolite composition. Results: To better understand the effect of “place” on berry ripening, transcript abundances in Cabernet Sauvignon berries grown in Bordeaux were compared to those in Reno during the late stages of berry development at similar berry sugar levels (19 to 26 °Brix, total soluble solids (TSS)). Day lengths were similar in both locations but day temperatures were warmer and night temperatures were cooler in Reno. TSS was lower in Bordeaux berries compared to Reno at maturity levels considered optimum for harvest. RNA-seq analysis identified 4,455 differentially expressed genes (DEGs) between Bordeaux and Reno grape skins at 22°Brix. Top DEG gene ontology categories involved response to stimulus (1464 genes), biosynthesis (1260 genes) and response to stress (834 genes). Some DEGS included genes encoding terpene synthases, cell wall enzymes, kinases, transporters, transcription factors and photoreceptors. Most circadian clock genes had higher transcript abundance in Bordeaux. The plant temperature sensor phytochrome B was linked with Reveille 1 expression, which is part of the circadian clock output pathway that affects seed dormancy. Bordeaux berries had higher transcript abundance with DEGs associated with seed dormancy, light, auxin, ethylene signaling, powdery mildew infection, phenylpropanoid, carotenoid and terpenoid metabolism, whereas Reno berries were enriched with DEGs involved in water deprivation, cold response, ABA signaling and Fe homeostasis. Conclusions: Transcript abundance profiles in the berry skins at maturity were highly dynamic. RNA-seq analysis identified a common core set of ripening genes that do not depend on rootstock, vineyard management, plant age, soil and climatic conditions. Most DEGs could be associated with different environmental conditions that affected the berries in the two locations and may be potentially controlled in different ways by the vinegrower to adjust final berry composition and reach a desired result. Temperature, light, water status and fungal infection were identified to be some of the most influential factors that affected differential gene expression and the quality trait pathways associated with them.