Combined physiological, transcriptome, and cis-regulatory element analyses indicate that key aspects of ripening, metabolism, and transcriptional program in grapes (Vitis vinifera L.) are differentially modulated accordingly to fruit size

Abstract

BackgroundIn wine grape production, management practices have been adopted to optimize grape and wine quality attributes by producing, or screening for, berries of smaller size. Fruit size and composition are influenced by numerous factors that include both internal (e.g. berry hormone metabolism) and external (e.g. environment and cultural practices) factors. Combined physiological, biochemical, and transcriptome analyses were performed to improve our current understanding of metabolic and transcriptional pathways related to berry ripening and composition in berries of different sizes.ResultsThe comparison of berry physiology between small and large berries throughout development (from 31 to 121 days after anthesis, DAA) revealed significant differences in firmness, the rate of softening, and sugar accumulation at specific developmental stages. Small berries had significantly higher skin to berry weight ratio, lower number of seeds per berry, and higher anthocyanin concentration compared to large berries. RNA-sequencing analyses of berry skins at 47, 74, 103, and 121 DAA revealed a total of 3482 differentially expressed genes between small and large berries. Abscisic acid, auxin, and ethylene hormone pathway genes were differentially modulated between berry sizes. Fatty acid degradation and stilbenoid pathway genes were upregulated at 47 DAA while cell wall degrading and modification genes were downregulated at 74 DAA in small compared to large berries. In the late ripening stage, concerted upregulation of the general phenylpropanoid and stilbenoid pathway genes and downregulation of flavonoid pathway genes were observed in skins of small compared to large berries. Cis-regulatory element analysis of differentially expressed hormone, fruit texture, flavor, and aroma genes revealed an enrichment of specific regulatory motifs related to bZIP, bHLH, AP2/ERF, NAC, MYB, and MADS-box transcription factors.ConclusionsThe study demonstrates that physiological and compositional differences between berries of different sizes parallel transcriptome changes that involve fruit texture, flavor, and aroma pathways. These results suggest that, in addition to direct effects brought about by differences in size, key aspects involved in the regulation of ripening likely contribute to different quality profiles between small and large berries.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2660-z) contains supplementary material, which is available to authorized users.

Genetic, epigenetic and genomic effects on variation of gene expression among grape varieties

“…Berry transcriptomics has been widely used to study this diversity. Differential expression under contrasting conditions and coexpression networks have suggested candidate genes for developmental changes (Carbonell‐Bejerano et al ., ; Cramer et al ., ; Palumbo et al ., ; Wong et al ., ), responses to stimuli (Deluc et al ., ; Rienth et al ., ; Blanco‐Ulate et al ., ), and variation in metabolite composition (Dal Santo et al ., ; Zenoni et al ., ). Gene expression is usually analysed in one or a few genotypes per experiment, and genotypes usually differ between experiments.…”

Genome-wide analysis of cis-regulatory element structure and discovery of motif-driven gene co-expression networks in grapevine

“…The availability of the grapevine genome and the rapid accumulation of publicly available grapevine whole-genome microarray and RNA-seq datasets provide the raw material necessary for GCN and CRE analyses. To date, several studies have utilized GCN and CRE analyses in revealing biologically relevant target genes of grapevine TFs 28–30 and/or providing clues into the regulatory relationships of TFs in key metabolic and ripening pathways 31 , 32 . However, to date no study has characterized grapevine promoter architecture and identified putative CRE regulatory modules at a genome-wide scale.…”

Abnormal Endogenous Repression of GA Signaling in a Seedless Table Grape Cultivar with High Berry Growth Response to GA Application

“…Since seed traces of stenospermocarpic cultivar are considered the primary source of GA in the grape berry after endosperm abortion (Conde et al, 2007), it was envisioned that berry variations in bioactive GA content may be influenced by differences in size or presence of seed traces. Analyses of 100 30-day-old berries, sampled randomly from 20 clusters, revealed the presence of seed traces in all berries of SB, while berries of BF had no visible seed traces.…”

“…In berries, however, both growth response to PAC and endogenous bioactive GA measurements correlated with the response to GA. As suggested above, the lower level of GA in BF, which may further contribute to its high response to GA application, can be associated to the absence of seed traces, which are the main sources of bioactive GAs in stenospermocarpic cultivars (Conde et al, 2007). In agreement with this hypothesis, (1) the absence of seed traces in BF correlated with low levels of bioactive GA (both GA 1 and GA 4 ) in the berries; (2) the presence of seed traces in the berries of SB was accompanied by higher bioactive GA 4 quantities, possibly resulting from the upregulation of GA biosynthetic genes, VvGA20ox4 and VvGA3ox3 ( Figure 9 ).…”