Effect of water deficit on fruit metabolism in white and red grape varieties

Plants are sessile organisms and often they have to cope with environmental stresses (abiotic factors) such as drought, cold, heat, extreme light, excessive soil salinity, or several combinations of them. The genotype x environment (GxE) interaction is the source of the main variability in the responses to these constrains. Among the abiotic factors that can influence plant physiology, drought is the most relevant because it can influence plant growth and yield, and affects fruits composition. Secondary metabolism contributes to the adaptation of a plant to its environment. In fruit crops such as grapevine (Vitis vinifera L.), secondary metabolism also largely determines fruit quality. Grapevine is considered a drought-tolerant plant and traditionally is not irrigated, especially in Europe. Mediterranean climate, with warm and dry summers and cold and wet winters, is considered optimal for viticulture. Climate change is predicted to exacerbate drought events in several viticultural areas, potentially affecting the accumulation of secondary metabolites in the grapes, thus affecting wine quality.
\nWe adopted a multidisciplinary approach that considered a two-years field trial, high-throughput transcripts profiling (RNA-sequencing) and large-scale targeted metabolite analyses to investigate the effect of drought events on the berry metabolism during fruit development and ripening in white and red grape varieties. An open field experiment was therefore conducted on Tocai friulano (white grape variety) and Merlot (red grape variety) vines in 2011 and 2012, in a North Italian viticultural area characterized by transient drought events during the summer. Two irrigation treatments were applied to the vines: (i) control vines were weekly irrigated, in order to keep their stem water potential (a sensitive indicator of grapevine water status) between -0.4 and -0.6 MPa; (ii) deficit irrigated vines were not irrigated from fruit set to harvest except in case of acute water deficit. Merlot vines were sheltered with an open-sided transparent cover at the beginning of the seasons, while Tocai friulano vines were cultivated without any cover and hence subjected to the natural precipitations. In Merlot, deficit irrigated vines experienced water deficit from 40-50 days after anthesis in both seasons. In Tocai friulano, deficit irrigated vines manifested a late deficit (from 80-90 days after anthesis) in 2011, and a prolonged water deficit from early stages of fruit development (from 30-40 days after anthesis) to harvest in 2012. For both varieties, berries were sampled for transcript and metabolite analyses during berry development and ripening. Furthermore, at harvest, grapes were microvinificated and wines composition was evaluated focusing on the secondary metabolites that largely contribute to the final color, taste, and aromatic features.
\nA large effect of water deficit on fruit secondary metabolism of the white grape variety Tocai friulano was observed in the season when the deficit occurred from early stages of berry development to harvest. In this particularly season, increased concentrations of phenylpropanoids, monoterpenes, and tocopherols were observed, while carotenoid and flavonoid accumulations were differentially modulated by water deficit accordingly to the berry developmental stage. In parallel, RNA sequencing analysis revealed that many key genes of the phenylpropanoid, flavonoid, and terpenoid pathways were modulated by water deficit indicating a transcriptional regulation of these specific pathways in the berry under drought. The higher co-regulation of several terpenoid transcripts with monoterpene accumulation under water deficit and the enrichment of drought-responsive elements in the promoter region of many terpenoid genes highlight that drought can enhance the production of these flavour components in grapes with potential effects on wine composition and sensory features. The wines produced from grapes subjected to water deficit revealed a more pronounced accumulation of monoterpenes and C13-norisoprenoids, and especially glycosidically-bound compounds. However, differences in the metabolic response between seasons suggest that the endurance of water deficit and the timing of application strongly impact this response.
\nIn Merlot berries, the drought stress response encompassed both ABA-dependent and ABA-independent signal transduction pathways with several VviAREB/ABFs, VvibZIP, and VviAP2/ERF-DREB transcription factors that were up-regulated by water deficit at one or more developmental stages. These transcription factors can play critical roles in the drought response by modulating a large suite of genes. Analyses of the central and specialized berry metabolism was conducted both at the transcript and metabolite levels by investigating several metabolic pathways (glycolysis and sugar accumulation, tricarboxylic acid cycle and amino acid biosynthesis, phenylpropanoid, flavonoid, terpenes, carotenoids, and fatty acid degradation pathways). The study revealed that water deficit enhanced the accumulation of several osmoprotectants (proline, sucrose, and raffinose) and of secondary metabolites such as anthocyanins and C5, C7, C8, and C9 volatile organic compounds. Furthermore, a weighted gene co-expression network analysis clustered in a module several genes involved in the branched chain amino acids biosynthesis, phenylpropanoid and flavonoid pathways, and sugar derivative metabolism together with the transcription factors mentioned above involved in the drought-stress signal, indicating a putative role of these transcription factors on the regulation of the response of the fruit metabolism to drought in Merlot berries. The wines produced from grapes subjected to water deficit revealed a higher concentration of anthocyanins that determined higher color intensity and a bluer coloration of the wines.
\nA comparison between the two genotypes can be done only for the 2012 season, when levels and endurances of water deficit were similar between Tocai friulano and Merlot deficit irrigated vines. The data indicate that water deficit modulated the accumulation of several secondary compounds; however, the modulation of the secondary metabolism varied between cultivars indicating a genotype x environment interaction. In the Tocai friulano berry, water deficit specifically stimulated the synthesis of phenolic acids, such as gallic acid, ellagic acid, and caftaric acid, tocopherols, and monoterpenes, such as linalool, α-terpineol, nerol, and hotrienol. In Merlot, the response included an overproduction of anthocyanins, such as the tri-substituted delphinidin, petunidin, and malvidin both in the glycosylated and acylated form, and C5, C7, C8 and C9 volatile organic, such as 1-penten-3-ol, (E)-2-heptenal, (E)-2-octenal, 1-octen-3-ol, and nonanol. A common response between the two varieties included a higher accumulation of gallic acid, zeaxanthin, (E)-2-heptenal, (E)-2-octenal, 1-octen-3-ol, and nonanol in the berry. Furthermore, these results indicate that drought events can affect the composition and sensory features of white and red wines by increasing the accumulation of benzoic and cinnamic acids, pigments in the red grape variety and monoterpenes in the white grape variety

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