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, 60 (3), 853-67

Post-veraison Sunlight Exposure Induces MYB-mediated Transcriptional Regulation of Anthocyanin and Flavonol Synthesis in Berry Skins of Vitis Vinifera

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Post-veraison Sunlight Exposure Induces MYB-mediated Transcriptional Regulation of Anthocyanin and Flavonol Synthesis in Berry Skins of Vitis Vinifera

José Tomás Matus et al. J Exp Bot.

Abstract

Anthocyanins, flavan-3-ols, and flavonols are the three major classes of flavonoid compounds found in grape berry tissues. Several viticultural practices increase flavonoid content in the fruit, but the underlying genetic mechanisms responsible for these changes have not been completely deciphered. The impact of post-veraison sunlight exposure on anthocyanin and flavonol accumulation in grape berry skin and its relation to the expression of different transcriptional regulators known to be involved in flavonoid synthesis was studied. Treatments consisting of removing or moving aside the basal leaves which shade berry clusters were applied. Shading did not affect sugar accumulation or gene expression of HEXOSE TRANSPORTER 1, although in the leaf removal treatment, these events were retarded during the first weeks of ripening. Flavonols were the most drastically reduced flavonoids following shading and leaf removal treatments, related to the reduced expression of FLAVONOL SYNTHASE 4 and its putative transcriptional regulator MYB12. Anthocyanin accumulation and the expression of CHS2, LDOX, OMT, UFGT, MYBA1, and MYB5a genes were also affected. Other regulatory genes were less affected or not affected at all by these treatments. Non-transcriptional control mechanisms for flavonoid synthesis are also suggested, especially during the initial stages of ripening. Although berries from the leaf removal treatment received more light than shaded fruits, malvidin-3-glucoside and total flavonol content was reduced compared with the treatment without leaf removal. This work reveals that flavonol-related gene expression responds rapidly to field changes in light levels, as shown by the treatment in which shaded fruits were exposed to light in the late stages of ripening. Taken together, this study establishes MYB-specific responsiveness for the effect of sun exposure and sugar transport on flavonoid synthesis.

Figures

Fig. 1.
Fig. 1.
Simplified overview of flavonol and anthocyanin biosynthesis within the phenylpropanoid pathway and its regulation in grape by characterized MYB genes (flavan-3-ols are not shown in this pathway). The repressor MYB4 is shown in red, while all MYB activators are shown in green. Abbreviations: CHS, chalcone synthase; CHI, chalcone isomerase; F3H/F3′H/F3′5′H, flavonoid hydroxylases; DFR, dihydroflavonol-4-reductase; ANS/LDOX, anthocyanidin synthase/leucoanthocyanidin dioxygenase; UFGT, UDP glucose:flavonoid-3-O-glucosyltransferase; FLS, flavonol synthase; and OMT, O-methyltransferase. (This figure is available in colour at JXB online.)
Fig. 2.
Fig. 2.
(A) Experimental design and data sampling for different light exposure and leaf removal treatments. Coloured clusters represent the grape phenologies observed during the different periods of ripening. Even-numbered weeks (squares) were sampled for HPLC flavonoid analysis, while odd-numbered weeks (asterisks) were sampled for RNA extraction and gene expression quantification. Symbols on the right correspond to each treatment as used in Figs 4–7. (B) Field photograph of grapes before and after T3 treatment (leaves were moved aside but not removed). (This figure is available in colour at JXB online.)
Fig. 3.
Fig. 3.
PAR measurements taken at 4 weeks after veraison for shaded and exposed clusters from the east side of one of the experimental rows. Incident PAR is included. (A) Arrow indicates the position of the PAR meter in each cluster. (B) Daily measurements from 08.00 h to 18.00 h.
Fig. 4.
Fig. 4.
Concentration of total and 3-O-glycosylated anthocyanin compounds from the different light exposure treated berry skins, taken from 2–8 weeks after veraison. (filled inverted triangles) T1 exposed; (open circles) T2 delayed; (filled circles) T3 shaded; (open triangles) T4 leaf removal. Anthocyanin concentrations are calculated in malvidin equivalents. Vertical bars indicate the standard deviation (three biological replicates). Different letters indicate significant differences between treatments as calculated by Tukey statistical analysis (P <0.05).
Fig. 5.
Fig. 5.
Changes in the expression of anthocyanin biosynthetic genes, the MYBA regulator and HEXOSE TRANSPORTER1, under different light exposure or leaf removal treatments. (filled inverted triangles) T1 exposed; (open circles) T2 delayed; (closed circles) T3 shaded; (open triangles) T4 leaf removal. Transcript levels are expressed in relation to the VvUBIQUITIN1 gene. Vertical bars indicate the standard deviation (three biological replicates). Different letters indicate significant differences between treatments as calculated by Tukey statistical analysis (P <0.05).
Fig. 6.
Fig. 6.
Changes in transcript levels of MYB, MYC, and WDR regulators of different branches of flavonoid synthesis, under different light exposure or leaf removal treatments. (filled inverted triangles) T1 exposed; (open circles) T2 delayed; (filled circles) T3 shaded; (open triangles) T4 leaf removal. Transcript levels are expressed in relation to the VvUBIQUITIN1 gene. Vertical bars indicate the standard deviation (three biological replicates). Different letters indicate significant differences between treatments as calculated by Tukey statistical analysis (P <0.05).
Fig. 7.
Fig. 7.
Changes in total berry skin flavonol content (A) and transcription levels of the flavonol biosynthetic gene FLS4 and its putative regulator MYB12 (B) under different light exposure or leaf removal treatments. (filled inverted triangles) T1 exposed; (open circles) T2 delayed; (filled circles) T3 shaded; (open triangles) T4 leaf removal. Vertical bars indicate the standard deviation (three biological replicates). Different letters indicate significant differences between treatments for each ripening stage as calculated by Tukey statistical analysis (P <0.05).

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