BackgroundGrapevine metabolism in response to water deficit was studied in two cultivars, Shiraz and Cabernet Sauvignon, which were shown to have different hydraulic behaviors (Hochberg et al. Physiol. Plant. 147:443–453, 2012).ResultsProgressive water deficit was found to effect changes in leaf water potentials accompanied by metabolic changes. In both cultivars, but more intensively in Shiraz than Cabernet Sauvignon, water deficit caused a shift to higher osmolality and lower C/N ratios, the latter of which was also reflected in marked increases in amino acids, e.g., Pro, Val, Leu, Thr and Trp, reductions of most organic acids, and changes in the phenylpropanoid pathway. PCA analysis showed that changes in primary metabolism were mostly associated with water stress, while diversification of specialized metabolism was mostly linked to the cultivars. In the phloem sap, drought was characterized by higher ABA concentration and major changes in benzoate levels coinciding with lower stomatal conductance and suberinization of vascular bundles. Enhanced suberin biosynthesis in Shiraz was reflected by the higher abundance of sap hydroxybenzoate derivatives. Correlation-based network analysis revealed that compared to Cabernet Sauvignon, Shiraz had considerably larger and highly coordinated stress-related changes, reflected in its increased metabolic network connectivity under stress. Network analysis also highlighted the structural role of major stress related metabolites, e.g., Pro, quercetin and ascorbate, which drastically altered their connectedness in the Shiraz network under water deficit.ConclusionsTaken together, the results showed that Vitis vinifera cultivars possess a common metabolic response to water deficit. Central metabolism, and specifically N metabolism, plays a significant role in stress response in vine. At the cultivar level, Cabernet Sauvignon was characterized by milder metabolic perturbations, likely due to a tighter regulation of stomata upon stress induction. Network analysis was successfully implemented to characterize plant stress molecular response and to identify metabolites with a significant structural and biological role in vine stress response.
BackgroundGrapevine berries undergo complex biochemical changes during fruit maturation, many of which are dependent upon the variety and its environment. In order to elucidate the varietal dependent developmental regulation of primary and specialized metabolism, berry skins of Cabernet Sauvignon and Shiraz were subjected to gas chromatography–mass spectrometry (GC-MS) and liquid chromatography–mass spectrometry (LC-MS) based metabolite profiling from pre-veraison to harvest. The generated dataset was augmented with transcript profiling using RNAseq.ResultsThe analysis of the metabolite data revealed similar developmental patterns of change in primary metabolites between the two cultivars. Nevertheless, towards maturity the extent of change in the major organic acid and sugars (i.e. sucrose, trehalose, malate) and precursors of aromatic and phenolic compounds such as quinate and shikimate was greater in Shiraz compared to Cabernet Sauvignon. In contrast, distinct directional projections on the PCA plot of the two cultivars samples towards maturation when using the specialized metabolite profiles were apparent, suggesting a cultivar-dependent regulation of the specialized metabolism. Generally, Shiraz displayed greater upregulation of the entire polyphenol pathway and specifically higher accumulation of piceid and coumaroyl anthocyanin forms than Cabernet Sauvignon from veraison onwards. Transcript profiling revealed coordinated increased transcript abundance for genes encoding enzymes of committing steps in the phenylpropanoid pathway. The anthocyanin metabolite profile showed F3′5′H-mediated delphinidin-type anthocyanin enrichment in both varieties towards maturation, consistent with the transcript data, indicating that the F3′5′H-governed branching step dominates the anthocyanin profile at late berry development. Correlation analysis confirmed the tightly coordinated metabolic changes during development, and suggested a source-sink relation between the central and specialized metabolism, stronger in Shiraz than Cabernet Sauvignon. RNAseq analysis also revealed that the two cultivars exhibited distinct pattern of changes in genes related to abscisic acid (ABA) biosynthesis enzymes.ConclusionsCompared with CS, Shiraz showed higher number of significant correlations between metabolites, which together with the relatively higher expression of flavonoid genes supports the evidence of increased accumulation of coumaroyl anthocyanins in that cultivar. Enhanced stress related metabolism, e.g. trehalose, stilbene and ABA in Shiraz berry-skin are consistent with its relatively higher susceptibility to environmental cues.
Grapes are one of the major fruit crops and they are cultivated in many dry environments. This study comprehensively characterizes the metabolic response of grape berries exposed to water deficit at different developmental stages. Increases of proline, branched-chain amino acids, phenylpropanoids, anthocyanins, and free volatile organic compounds have been previously observed in grape berries exposed to water deficit. Integrating RNA-sequencing analysis of the transcriptome with large-scale analysis of central and specialized metabolites, we reveal that these increases occur via a coordinated regulation of key structural pathway genes. Water deficit-induced up-regulation of flavonoid genes is also coordinated with the down-regulation of many stilbene synthases and a consistent decrease in stilbenoid concentration. Water deficit activated both ABA-dependent and ABA-independent signal transduction pathways by modulating the expression of several transcription factors. Gene-gene and gene-metabolite network analyses showed that water deficit-responsive transcription factors such as bZIPs, AP2/ERFs, MYBs, and NACs are implicated in the regulation of stress-responsive metabolites. Enrichment of known and novel cis-regulatory elements in the promoters of several ripening-specific/water deficit-induced modules further affirms the involvement of a transcription factor cross-talk in the berry response to water deficit. Together, our integrated approaches show that water deficit-regulated gene modules are strongly linked to key fruit-quality metabolites and multiple signal transduction pathways may be critical to achieve a balance between the regulation of the stress-response and the berry ripening program. This study constitutes an invaluable resource for future discoveries and comparative studies, in grapes and other fruits, centered on reproductive tissue metabolism under abiotic stress.
Drought stress is known to limit photosynthesis rates and to inflict photo-oxidative damage in grapevines. Grapevines, which are considered drought-tolerant plants, are characterized by diverse hydraulic and photosynthetic behaviors, depending on the cultivar. This research compared the photosynthesis and the photorespiration of Cabernet Sauvignon (Cs) (isohydric) and Shiraz (anisohydric) in an attempt to acquire a wider perspective on the iso/anisohydric phenomenon and its implications. Shiraz and Cs were subjected to terminal drought in the greenhouse. Soil water content (θ), leaf water potential (Ψl ) and stomata conductance (gs ) were measured to determine the cultivars' hydraulic behavior. Gas exchange and fluorometry measurements were taken at 21 and 2% O2 to acquire photosynthesis and photorespiration characteristics. Cs was found to behave in a near isohydric manner whereas Shiraz behaved in a near anisohydric manner. Compared to Shiraz, the reduced stomata conductance values of Cs were accompanied by higher water use efficiency and photorespiration rates, as well as photosystem II photochemical potential (Fv /Fm ). As compared with Shiraz, Cs compensated for lower stomata conductance by higher photosynthesis and photorespiration. These two processes contributed to higher electron flow rates that might have a role in photoinhibition avoidance, which was observed in the stability of Fv /Fm under drought stress.
Background Grapevine is an economically important crop for which yield and berry quality is strongly affected by climate change. Large variations in drought tolerance exist across Vitis species. Some of these species are used as rootstock to enhance abiotic and biotic stress tolerance. In this study, we investigated the physiological and transcriptomic responses to water deficit of four different genotypes that differ in drought tolerance: Ramsey (Vitis champinii), Riparia Gloire (Vitis riparia), Cabernet Sauvignon (Vitis vinifera), and SC2 (Vitis vinifera x Vitis girdiana). Results Ramsey was particularly more drought tolerant than the other three genotypes. Ramsey maintained a higher stomatal conductance and photosynthesis at equivalent levels of moderate water deficit. We identified specific and common transcriptomic responses shared among the four different Vitis species using RNA sequencing analysis. A weighted gene co-expression analysis identified a water deficit core gene set with the ABA biosynthesis and signaling genes, NCED3, RD29B and ABI1 as potential hub genes. The transcript abundance of many abscisic acid metabolism and signaling genes was strongly increased by water deficit along with genes associated with lipid metabolism, galactinol synthases and MIP family proteins. This response occurred at smaller water deficits in Ramsey and with higher transcript abundance than the other genotypes. A number of aquaporin genes displayed differential and unique responses to water deficit in Ramsey leaves. Genes involved in cysteine biosynthesis and metabolism were constitutively higher in the roots of Ramsey; thus, linking the gene expression of a known factor that influences ABA biosynthesis to this genotype’s increased NCED3 transcript abundance. Conclusion The drought tolerant Ramsey maintained higher photosynthesis at equivalent water deficit than the three other grapevine genotypes. Ramsey was more responsive to water deficit; its transcriptome responded at smaller water deficits, whereas the other genotypes did not respond until more severe water deficits were reached. There was a common core gene network responding to water deficit for all genotypes that included ABA metabolism and signaling. The gene clusters and sub-networks identified in this work represent interesting gene lists to explore and to better understand drought tolerance molecular mechanisms.
Main conclusion Drought-acclimated vines maintained higher gas exchange compared to irrigated controls under water deficit; this effect is associated with modified leaf turgor but not with improved petiole vulnerability to cavitation. A key feature for the prosperity of plants under changing environments is the plasticity of their hydraulic system. In the present research we studied the hydraulic regulation in grapevines (Vitis vinifera L.) that were first acclimated for 39 days to well-watered (WW), sustained water deficit (SD), or transient—cycles of dehydration–rehydration—water deficit (TD) conditions, and then subjected to varying degrees of drought. Vine development under SD led to the smallest leaves and petioles, but the TD vines had the smallest mean xylem vessel and calculated specific conductivity (k ts). Unexpectedly, both the water deficit acclimation treatments resulted in vines more vulnerable to cavitation in comparison to WW, possibly as a result of developmental differences or cavitation fatigue. When exposed to drought, the SD vines maintained the highest stomatal (g s) and leaf conductance (k leaf) under low stem water potential (Ψs), despite their high xylem vulnerability and in agreement with their lower turgor loss point (ΨTLP). These findings suggest that the down-regulation of k leaf and g s is not associated with embolism, and the ability of drought-acclimated vines to maintain hydraulic conductance and gas exchange under stressed conditions is more likely associated with the leaf turgor and membrane permeability.Electronic supplementary materialThe online version of this article (doi:10.1007/s00425-017-2662-3) contains supplementary material, which is available to authorized users.
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