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Anthocyanin biosynthesis is differentially regulated by light in the skin and flesh of white-fleshed and teinturier grape berries

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Abstract

Main conclusion

Light exclusion reduces the concentration and modifies the composition of grape anthocyanins, by altering the expression of genes involved in anthocyanin biosynthesis and transport, in a cultivar- and tissue-specific manner.

Unlike most grapes, teinturier grapes accumulate anthocyanins both in skin and flesh. However, the concentration and composition of anthocyanins in both tissues differ, providing a valuable system to study tissue-specific regulation of anthocyanin synthesis. Furthermore, little is known about the mechanisms controlling the sensitivity of anthocyanin accumulation to light. Here, light was excluded from Gamay (white-fleshed) and Gamay Fréaux (teinturier mutant) berries throughout berry development. Under light-exposed conditions, the skin of Gamay Fréaux accumulated the highest level of anthocyanins, followed by the skin of Gamay, while the pulp of Gamay Fréaux had much lower anthocyanins than the skins. Network analysis revealed the same order on the number of significant correlations among metabolites and transcripts in the three colored tissues, indicating a higher connectivity that reflects a higher efficiency of the anthocyanin pathway. Compared to light conditions, light exclusion reduced the total amount of anthocyanins, most severely in the skin of Gamay and to a lesser extent in the flesh and skin of Gamay Fréaux. Coordinated decrease in the transcript abundance of structural, regulatory and transporter genes by light exclusion correlated with the reduced anthocyanin concentration in a cultivar- and tissue-specific manner. Moreover, light exclusion increased the ratio of dihydroxylated to trihydroxylated anthocyanins, in parallel with F3′H and F3′5′H transcript amounts. Sugars and ABA only play a limited role in the control of anthocyanin synthesis in the berries, in contrast with what has been described in cell suspensions. This study provides novel insights into the regulation of anthocyanin in wild type and teinturier cultivars.

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Abbreviations

ABA:

Abscisic acid

AM1:

Anthocyanin multidrug and toxic extrusion (MATE)-type transporter 1

AM3:

Anthocyanin multidrug and toxic extrusion (MATE)-type transporter 3

AOMT:

Anthocyanin O-methyltransferase

CHI:

Chalcone isomerase

CHS:

Chalcone synthase

Cy:

Cyanidin

CytoB5:

Cytochrome b5

DAF:

Days after flowering

DFR:

Dihydroflavonol reductase

F3′5′H:

Flavonoid 3′,5′-hydroxylase

F3′H:

Flavonoid 3′-hydroxylase

GST:

Glutathione S-transferase

NCED:

9-Cis-epoxycarotenoid dioxygenase

PCA:

Principal component analysis

Pn:

Peonidin

UFGT:

UDP-glucose flavonoid 3-O-glucosyltransferase

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Acknowledgments

The authors thank the Eiffel Fellowship program for supporting LG’s stay in France. We thank Fatma Lecourieux, David Lecourieux, and Pierre Helwi for help in qPCR analysis; We also thank Virginie Lauvergeat for critically reviewing the manuscript.

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    1. UMR 1287 EGFV, INRA, Univ. de Bordeaux, ISVV, 33882, Villenave d’Ornon, France

      Le Guan, Zhanwu Dai, Jing Wu, Isabelle Merlin, Ghislaine Hilbert, Christel Renaud, Eric Gomès & Serge Delrot

    2. Beijing Key Laboratory of Grape Science and Enology, and CAS Key Laboratory of Plant Resources, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China

      Le Guan, Ben-Hong Wu & Shao-Hua Li

    3. Commonwealth Scientific and Industrial Research Organisation, Agriculture Flagship, PMB2, Glen Osmond, SA, 5064, Australia

      Everard Edwards

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    Guan, L., Dai, Z., Wu, BH. et al. Anthocyanin biosynthesis is differentially regulated by light in the skin and flesh of white-fleshed and teinturier grape berries. Planta 243, 23–41 (2016). https://doi.org/10.1007/s00425-015-2391-4

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