Multi-Omics and Integrated Network Analyses Reveal New Insights into the Systems Relationships between Metabolites, Structural Genes, and Transcriptional Regulators in Developing Grape Berries (Vitis vinifera L.) Exposed to Water Deficit.

Front Plant Sci. 2017 Jul 10;8:1124. doi: 10.3389/fpls.2017.01124. eCollection 2017. Savoi S1,2, Wong DCJ3, Degu A4, Herrera JC1, Bucchetti B1, Peterlunger E1, Fait A4, Mattivi F2,5, Castellarin SD3. Author information 1 Department of Agricultural, Food, Environmental and Animal Sciences, University of UdineUdine, Italy. 2 Department of Food Quality and Nutrition, Research and Innovation Centre, Fondazione Edmund MachSan Michele all'Adige, Italy. 3 Wine Research Centre, The University of British Columbia, VancouverBC, Canada. 4 The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the NegevSede Boqer, Israel. 5 Center Agriculture Food Environment, University of TrentoSan Michele all'Adige, Italy. Abstract 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. KEYWORDS: RNA-sequencing; abiotic stress; central metabolism; drought; fruit quality; grapevine; ripening; specialized metabolism PMID: 28740499 PMCID: PMC5502274 DOI: 10.3389/fpls.2017.01124 Free PMC Article Images from this publication.See all images (8)Free text