Temperature desynchronizes sugar and organic acid metabolism in ripening grapevine fruits and remodels their transcriptome

Abstract

BackgroundFruit composition at harvest is strongly dependent on the temperature during the grapevine developmental cycle. This raises serious concerns regarding the sustainability of viticulture and the socio-economic repercussions of global warming for many regions where the most heat-tolerant varieties are already cultivated. Despite recent progress, the direct and indirect effects of temperature on fruit development are far from being understood. Experimental limitations such as fluctuating environmental conditions, intra-cluster heterogeneity and the annual reproductive cycle introduce unquantifiable biases for gene expression and physiological studies with grapevine. In the present study, DRCF grapevine mutants (microvine) were grown under several temperature regimes in duly-controlled environmental conditions. A singly berry selection increased the accuracy of fruit phenotyping and subsequent gene expression analyses. The physiological and transcriptomic responses of five key stages sampled simultaneously at day and nighttime were studied by RNA-seq analysis.ResultsA total of 674 millions reads were sequenced from all experiments. Analysis of differential expression yielded in a total of 10 788 transcripts modulated by temperature. An acceleration of green berry development under higher temperature was correlated with the induction of several candidate genes linked to cell expansion. High temperatures impaired tannin synthesis and degree of galloylation at the transcriptomic levels. The timing of malate breakdown was delayed to mid-ripening in transgressively cool conditions, revealing unsuspected plasticity of berry primary metabolism. Specific ATPases and malate transporters displayed development and temperature-dependent expression patterns, besides less marked but significant regulation of other genes in the malate pathway.ConclusionThe present study represents, to our knowledge the first abiotic stress study performed on a fleshy fruits model using RNA-seq for transcriptomic analysis. It confirms that a careful stage selection and a rigorous control of environmental conditions are needed to address the long-term plasticity of berry development with respect to temperature. Original results revealed temperature-dependent regulation of key metabolic processes in the elaboration of berry composition. Malate breakdown no longer appears as an integral part of the veraison program, but as possibly triggered by an imbalance in cytoplasmic sugar, when efficient vacuolar storage is set on with ripening, in usual temperature conditions. Furthermore, variations in heat shock responsive genes that will be very valuable for further research on temperature adaptation of plants have been evidenced.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-016-0850-0) contains supplementary material, which is available to authorized users.

A Prunus persica genome‐wide RNA‐seq approach uncovers major differences in the transcriptome among chilling injury sensitive and non‐sensitive varieties

“…Temperature can have an important impact on the fruits transcriptome synchronization (Rienth et al ). In fact, prolonged cold exposure followed by room temperature storage incremented the synchronization of the four varieties transcriptome when compared to their patterns upon regular fruit ripening (Fig.…”

Genome-wide characterisation and expression profile of the grapevine ATL ubiquitin ligase family reveal biotic and abiotic stress-responsive and development-related members

“…Experiments included grapevine plants infected with Grapevine rupestris stem pitting-associated virus (GRSPaV)88, Botrytis cinerea 8990, Erysiphe necator 58, Neofusicoccum parvum 91, Plasmopara viticola 4192, Eutypa lata (Unpublished Microarray Nimblegen), or infested with the spider mite Tetranyhus urticae 60, and grapevine plants subjected to different abiotic stresses, namely drought stress in cv. Tocai berries during development and ripening93, berry cultures treated with exogenous glucose94, heat stress/acclimation in berries during berry development and ripening95, carbon starvation due to plant shading at bloom in flowers/inflorescences96 and UV-C treatment of berry skins97. Differential gene expression re-analysis based on the microarray and RNA-seq data was carried out using limma 98 and DESeq2 99, respectively, at FDR values < 0.05.…”

Agronomical and Chemical Effects of the Timing of Cluster Thinning on Pinot Noir (Clone 115) Grapes and Wines

“…While bloom + 12 fruit did have significantly lower pH than control fruit (Table 3), after accounting for growing season in the model, the effect of cluster thinning treatment was not significant, indicating that the climatic conditions prevalent during the growing season had a greater effect on fruit pH and TA than cluster thinning timing. The decrease of malate concentration in grapes post-véraison through respiration increases with temperature and light exposure [56,57]; as such, the decrease in TA and the corresponding increase in pH observed in 2017, which was the warmer season (Table A2), is likely a function of the increased temperature. There was a significant treatment × growing season interaction found in TA (Table 3).…”