Abstract
Main conclusion
White-fleshed grape cv. ‘Gamay’ and its two teinturier variants presented distinct spatial–temporal accumulation of anthocyanins, with uncoupled accumulation of sugars and anthocyanins in ‘Gamay Fréaux’.
Abstract
In most red grape cultivars, anthocyanins accumulate exclusively in the berry skin, while ‘teinturier’ cultivars also accumulate anthocyanins in the pulp. Here, we investigated the teinturier cvs. ‘Gamay de Bouze’ and ‘Gamay Fréaux’ (two somatic variants of the white-fleshed cv. ‘Gamay’) through metabolic and transcript analysis to clarify whether these two somatic variants have the same anthocyanin accumulation pattern in the skin and pulp, and whether primary metabolites are also affected. The skin of the three cultivars and the pulp of ‘Gamay de Bouze’ begun to accumulate anthocyanins at the onset of berry ripening. However, the pulp of ‘Gamay Fréaux’ exhibited a distinct anthocyanin accumulation pattern, starting as early as fruit set with very low level of sugars. The highest level of anthocyanins was found in ‘Gamay Fréaux’ skin, followed by ‘Gamay de Bouze’ and ‘Gamay’. Consistently, the transcript abundance of genes involved in anthocyanin biosynthesis were in line with the anthocyanin levels in the three cultivars. Despite no evident differences in pulp sugar content, the concentration of glucose and fructose in the skin of ‘Gamay Fréaux’ was only half of those in the skin of ‘Gamay’ and ‘Gamay de Bouze’ throughout all berry ripening, suggesting an uncoupled accumulation of sugars and anthocyanins in ‘Gamay Fréaux’. The study provides a comprehensive view of metabolic consequences in grape somatic variants and the three almost isogenic genotypes can serve as ideal reagents to further uncover the mechanisms underlying the linkage between sugar and anthocyanin accumulation.
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Abbreviations
- AOMT:
-
Anthocyanin O-methyltransferase
- CYTOB5:
-
Cytochrome b5
- DAF:
-
Days after flowering
- DFR:
-
Dihydroflavonol reductase
- F3′5′H:
-
Flavonoid 3′, 5′-hydroxylase
- F3′H:
-
Flavonoid 3′-hydroxylase
- UFGT:
-
UDP glucose: flavonoid-3-O-glucosyltransferase
References
Ageorges A, Fernandez L, Vialet S, Merdinoglu D, Terrier N, Romieu C (2006) Four specific isogenes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries. Plant Sci 170(2):372–383. https://doi.org/10.1016/j.plantsci.2005.09.007
Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J (2004) Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. New Phytol 164(1):157–164. https://doi.org/10.1111/j.1469-8137.2004.01157.x
Bell SJ, Henschke PA (2005) Implications of nitrogen nutrition for grapes, fermentation and wine. Aust J Grape Wine Res 11:242–295
Bobeica N, Poni S, Hilbert G, Renaud C, Gomes E, Delrot S, Dai Z (2015) Differential responses of sugar, organic acids and anthocyanins to source-sink modulation in Cabernet Sauvignon and Sangiovese grapevines. Front Plant Sci 6:382. https://doi.org/10.3389/fpls.2015.00382
Bogs J, Ebadi A, McDavid D, Robinson SP (2006) Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development. Plant Physiol 140(1):279–291. https://doi.org/10.1104/pp.105.073262
Boss PK, Davies C, Robinson SP (1996) Expression of anthocyanin biosynthesis pathway genes in red and white grapes. Plant Mol Biol 32:565–569
Castañeda-Ovando A, Pacheco-Hernández MdL, Páez-Hernández ME, Rodríguez JA, Galán-Vidal CA (2009) Chemical studies of anthocyanins: a review. Food Chem 113(4):859–871. https://doi.org/10.1016/j.foodchem.2008.09.001
Castellarin SD, Gambetta GA, Wada H, Shackel KA, Matthews MA (2011) Fruit ripening in vitis vinifera: spatiotemporal relationships among turgor, sugar accumulation, and anthocyanin biosynthesis. J Exp Bot 62(12):4345–4354. https://doi.org/10.1093/jxb/err150
Castillo-Munoz N, Fernandez-Gonzalez M, Gomez-Alonso S, Garcia-Romero E, Hermosin-Gutierrez I (2009) Red-color related phenolic composition of Garnacha Tintorera (Vitis vinifera L.) grapes and red wines. J Agric Food Chem 57(17):7883–7891. https://doi.org/10.1021/jf9002736
D’Onofrio C, Tumino G, Gardiman M, Crespan M, Bignami C, de Palma L, Barbagallo MG, Muganu M, Morcia C, Novello V, Schneider A, Terzi V (2021) Parentage atlas of Italian grapevine varieties as inferred from SNP genotyping. Front Plant Sci 11:605934
Dai ZW, Leon C, Feil R, Lunn JE, Delrot S, Gomes E (2013) Metabolic profiling reveals coordinated switches in primary carbohydrate metabolism in grape berry (Vitis vinifera L.), a non-climacteric fleshy fruit. J Exp Bot 64:1345–1355
Dai ZW, Meddar M, Renaud C, Merlin I, Hilbert G, Delrot S, Gomès E (2014) Long-term in vitro culture of grape berries and its application to assess the effects of sugar supply on anthocyanin accumulation. J Exp Bot 65(16):4665–4677. https://doi.org/10.1093/jxb/ert489
Dimitrovska M, Bocevska M, Dimitrovski D, Murkovic M (2011) Anthocyanin composition of Vranec, Cabernet Sauvignon, Merlot and Pinot Noir grapes as indicator of their varietal differentiation. Eur Food Res Technol 232(4):591–600. https://doi.org/10.1007/s00217-011-1425-9
Durán-Soria S, Pott DM, Osorio S, Vallarino JG (2020) Sugar signaling during fruit ripening. Front Plant Sci. https://doi.org/10.3389/fpls.2020.564917
Esteban M, Villanueva MJ, Lissarrague JR (2001) Effect of irrigation on changes in the anthocyanin composition of the skin of cv Tempranillo (Vitis vinifera L) grape berries during ripening. J Sci Food Agric 81:409–420
Fasoli M, Dal Santo S, Zenoni S, Tornielli GB, Farina L, Zamboni A, Porceddu A, Venturini L, Bicego M, Murino V, Ferrarini A, Delledonne M, Pezzotti M (2012) The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24(9):3489–3505. https://doi.org/10.1105/tpc.112.100230
Ferreira V, Pinto-Carnide O, Arroyo-García R, Castro I (2018) Berry color variation in grapevine as a source of diversity. Plant Physiol Biochem 132:696–707. https://doi.org/10.1016/j.plaphy.2018.08.021
Ferri M, Righetti L, Tassoni A (2011) Increasing sucrose concentrations promote phenylpropanoid biosynthesis in grapevine cell cultures. J Plant Physiol 168(3):189–195. https://doi.org/10.1016/j.jplph.2010.06.027
Fournier-Level A, Le Cunff L, Gomez C, Doligez A, Ageorges A, Roux C, Bertrand Y, Souquet JM, Cheynier V, This P (2009) Quantitative genetic bases of anthocyanin variation in grape (Vitis vinifera L. ssp. sativa) berry: a quantitative trait locus to quantitative trait nucleotide integrated study. Genetics 183(3):1127–1139. https://doi.org/10.1534/genetics.109.103929
Fournier-Level A, Hugueney P, Verries C, This P, Ageorges A (2011) Genetic mechanisms underlying the methylation level of anthocyanins in grape (Vitis vinifera L.). BMC Plant Biol 11:179. https://doi.org/10.1186/1471-2229-11-179
Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD (2010) Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232(1):219–234. https://doi.org/10.1007/s00425-010-1165-2
Gomez L, Bancel D, Rubio E, Vercambre G (2007) The microplate reader: an efficient tool for the separate enzymatic analysis of sugars in plant tissues—validation of a micro-method. J Sci Food Agric 87(10):1893–1905. https://doi.org/10.1002/jsfa.2924
Gonzalez-SanJose ML, Diez C (1992) Relationship between anthocyanins and sugars during the ripening of grape berries. Food Chem 43:193–197
Guan L, Li JH, Fan PG, Chen S, Fang JB, Li SH, Wu BH (2012) Anthocyanin accumulation in various organs of a teinturier cultivar (Vitis vinifera L.) during the growing season. Am J Enol Vitic 63(2):177–184. https://doi.org/10.5344/ajev.2011.11063
Guan L, Dai Z, Wu B-H, Wu J, Merlin I, Hilbert G, Renaud C, Gomès E, Edwards E, Li S-H, Delrot S (2015) Anthocyanin biosynthesis is differentially regulated by light in the skin and flesh of white-fleshed and teinturier grape berries. Planta 243(1):23–41. https://doi.org/10.1007/s00425-015-2391-4
He J-J, Liu Y-X, Pan Q-H, Cui X-Y, Duan C-Q (2010) Different anthocyanin profiles of the skin and the pulp of Yan73 (Muscat Hamburg × Alicante Bouschet) grape berries. Molecules 15(3):1141–1153. https://doi.org/10.3390/molecules15031141
Hernández-Orte P, Cacho JF, Ferreira V (2002) Relationship between varietal amino acid profile of grapes and wine aromatic composition. Experiments with model solutions and chemometric study. J Agric Food Chem 50:2891–2899
Hichri I, Heppel SC, Pillet J, Leon C, Czemmel S, Delrot S, Lauvergeat V, Bogs J (2010) The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine. Mol Plant 3(3):509–523. https://doi.org/10.1093/mp/ssp118
Hiratsuka S, Onodera H, Kawai Y, Kubo T, Itoh H, Wada R (2001) ABA and sugar effects on antocyanin formation in grape berry cultured in vitro. Sci Hortic 90:12–130
Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7(7):1071–1083. https://doi.org/10.1105/tpc.7.7.1071
Jia H, Wang Y, Sun M, Li B, Han Y, Zhao Y, Li X, Ding N, Li C, Ji W, Jia W (2013) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198(2):453–465. https://doi.org/10.1111/nph.12176
Kennedy J (2002) Understanding grape berry development. Practical Winery & Vineyard, USA
Kliewer WM (1965) Changes in concentration of glucose, fructose, and total soluble solids in flowers and berries of Vitis vinifera. Am J Enol Vitic 16:101–110
Kliewer WM (1966) Sugar and organic acids of Vitis vinifera. Plant Physiol 41:923–931
Kliewer WM (1967) The glucose-fructose ratio of Vitis Vinifera grapes. Am J Enol Vitic 18:33–41
Kliewer WM (1970) Free amino acids and other nitrogenous fractions in wine grapes. J Food Sci 35:17–21
Kobayashi S, Ishimaru M, Hiraoka K, Honda C (2002) Myb-related genes of the Kyoho grape ( Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215(6):924–933. https://doi.org/10.1007/s00425-002-0830-5
Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982. https://doi.org/10.1126/science.1095011
Koyama K, Sadamatsu K, Goto-Yamamoto N (2010) Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Funct Integr Genomics 10(3):367–381. https://doi.org/10.1007/s10142-009-0145-8
Koyama K, Ikeda H, Poudel PR, Goto-Yamamoto N (2012) Light quality affects flavonoid biosynthesis in young berries of Cabernet Sauvignon grape. Phytochemistry 78:54–64. https://doi.org/10.1016/j.phytochem.2012.02.026
Kuhn N, Guan L, Dai ZW, Wu B-H, Lauvergeat V, Gomès E, Li S-H, Godoy F, Arce-Johnson P, Delrot S (2013) Berry ripening: recently heard through the grapevine. J Exp Bot 65(16):4543–4559. https://doi.org/10.1093/jxb/ert395
Lamikanra O, Inyang ID, Leong S (1995) Distribution and effect of grape maturity on organic acid content of red Muscadine grapes. J Agric Food Chem 43(12):3026–3028. https://doi.org/10.1021/jf00060a007
Larronde F, Krisa S, Decendit A, Chèze C, Deffieux G, Mérillon JM (1998) Regulation of polyphenol production in Vitis vinifera cell suspension cultures by sugars. Plant Cell Rep 17:946–950
Laucou V, Launay A, Bacilieri R, Lacombe T, Adam-Blondon A-F, Bérard A, Chauveau A, de Andrés MT, Hausmann L, Ibáñez J, Le Paslier M-C, Maghradze D, Martinez-Zapater JM, Maul E, Ponnaiah M, Töpfer R, Péros J-P, Boursiquot J-M (2018) Extended diversity analysis of cultivated grapevine Vitis vinifera with 10K genome-wide SNPs. PLoS ONE 13:e0192540
Liang Z, Wu B, Fan P, Yang C, Duan W, Zheng X, Liu C, Li S (2008) Anthocyanin composition and content in grape berry skin in Vitis germplasm. Food Chem 111(4):837–844. https://doi.org/10.1016/j.foodchem.2008.04.069
Liu H-F, Wu B-H, Fan P-G, Li S-H, Li L-S (2006) Sugar and acid concentrations in 98 grape cultivars analyzed by principal component analysis. J Sci Food Agric 86(10):1526–1536. https://doi.org/10.1002/jsfa.2541
Liu XJ, An XH, Liu X, Hu DG, Wang XF, You CX, Hao YJ (2017) MdSnRK1.1 interacts with MdJAZ18 to regulate sucrose-induced anthocyanin and proanthocyanidin accumulation in apple. J Exp Bot 68(11):2977–2990. https://doi.org/10.1093/jxb/erx150
Mattivi F, Guzzon R, Vrhovsek U, Stefanini M, Velasco R (2006) Metabolite profiling of grape: flavonols and anthocyanins. J Agric Food Chem 54:7692–7702
Matus JT, Cavallini E, Loyola R, Höll J, Finezzo L, Dal Santo S, Vialet S, Commisso M, Roman F, Schubert A, Alcalde JA, Bogs J, Ageorges A, Tornielli GB, Arce-Johnson P (2017) A group of grapevine MYBA transcription factors located in chromosome 14 control anthocyanin synthesis in vegetative organs with different specificities compared with the berry color locus. Plant J 91(2):220–236. https://doi.org/10.1111/tpj.13558
Mullins MG, Rajasekaran K (1981) Fruit cutting: revisedmethod for producing test plants of grapevine cultivars. Am J Enol Vitic 32:35–40
Nardozza S, Boldingh HL, Kashuba MP, Feil R, Jones D, Thrimawithana AH, Ireland HS, Philippe M, Wohlers MW, McGhie TK, Montefiori M, Lunn JE, Allan AC, Richardson AC (2019) Carbon starvation reduces carbohydrate and anthocyanin accumulation in red-fleshed fruit via trehalose 6-phosphate and MYB27. Plant Cell Environ 43(4):819–835. https://doi.org/10.1111/pce.13699
Olivares D, Contreras C, Munoz V, Rivera S, Gonzalez-Aguero M, Retamales J, Defilippi BG (2017) Relationship among color development, anthocyanin and pigment-related gene expression in “Crimson Seedless” grapes treated with abscisic acid and sucrose. Plant Physiol Biochem 115:286–297. https://doi.org/10.1016/j.plaphy.2017.04.007
Ono E, Homma Y, Horikawa M, Kunikane-Doi S, Imai H, Takahashi S, Kawai Y, Ishiguro M, Fukui Y, Nakayama T (2010) Functional differentiation of the glycosyltransferases that contribute to the chemical diversity of bioactive flavonol glycosides in grapevines (Vitis vinifera). Plant Cell 22(8):2856–2871. https://doi.org/10.1105/tpc.110.074625
Pereira GE, Gaudillere JP, Pieri P, HILBert G, Maucourt M, Deborde C, Moing A, Rolin D (2006) Microclimate influence on mineral and metabolic profiles of grape berries. J Agric Food Chem 54:6765–6776
R Core Team (2007) R: a language and environment for statistical computing. https://www.R-project.org
Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27. https://doi.org/10.1186/1471-2229-6-27
Robles A, Fabjanowicz M, Chmiel T, Płotka-Wasylka J (2019) Determination and identification of organic acids in wine samples. Problems and challenges. Trends Anal Chem. https://doi.org/10.1016/j.trac.2019.115630
Röckel F, Moock C, Braun U, Schwander F, Cousins P, Maul E, Töpfer R, Hausmann L (2020) Color intensity of the red-fleshed berry phenotype of Vitis vinifera teinturier grapes varies due to a 408 bp duplication in the promoter of VvmybA1. Genes. https://doi.org/10.3390/genes11080891
Sadras VO, Moran MA (2012) Elevated temperature decouples anthocyanins and sugars in berries of Shiraz and Cabernet Franc. Aust J Grape Wine Res 18(2):115–122. https://doi.org/10.1111/j.1755-0238.2012.00180.x
Saigne-Soulard C, Richard T, Mérillon J-M, Monti J-P (2006) 13C NMR analysis of polyphenol biosynthesis in grape cells: impact of various inducing factors. Anal Chim Acta 563(1–2):137–144. https://doi.org/10.1016/j.aca.2005.09.073
Santibáñez C, Meyer C, Martínez L, Moyano T, Lunn J, Feil R, Dai Z, Carrasco D, Arroyo-García R, Hilbert G, Renaud C, Delrot S, Manke-Nachtigall F, Gutiérrez R, Matus JT, Gomès E, Arce-Johnson P (2019) Differences in berry primary and secondary metabolisms identified by transcriptomic and metabolic profiling of two table grape color somatic variants. bioRxiv. https://doi.org/10.1101/861120
Singh Brar H, Singh Z, Swinny E (2008) Dynamics of anthocyanin and flavonol profiles in the ‘Crimson Seedless’ grape berry skin during development and ripening. Sci Hortic 117(4):349–356. https://doi.org/10.1016/j.scienta.2008.05.007
Smeriglio A, Barreca D, Bellocco E, Trombetta D (2016) Chemistry, pharmacology and health benefits of anthocyanins. Phytother Res 30(8):1265–1286. https://doi.org/10.1002/ptr.5642
Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140(2):637–646. https://doi.org/10.1104/pp.105.072579
Soubeyrand E, Colombié S, Beauvoit B, Dai Z, Cluzet S, Hilbert G, Renaud C, Maneta-Peyret L, Dieuaide-Noubhani M, Mérillon J-M, Gibon Y, Delrot S, Gomès E (2018) Constraint-based modeling highlights cell energy, redox status and α-ketoglutarate availability as metabolic drivers for anthocyanin accumulation in grape cells under nitrogen limitation. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00421
Sweetman C, Sadras VO, Hancock RD, Soole KL, Ford CM (2014) Metabolic effects of elevated temperature on organic acid degradation in ripening Vitis vinifera fruit. J Exp Bot 65:5975–5988
Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Leon C, Renaudin J (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222:832–847
This P, Lacombe T, Thomas M (2006) Historical origins and genetic diversity of wine grapes. Trends Genet 22(9):511–519. https://doi.org/10.1016/j.tig.2006.07.008
Vitrac X, Larronde F, Krisa S, Decendit A, Deffieux G, Merillon JM (2000) Sugar sensing and Ca2+±calmodulin requirement in Vitis vinifera cells producing anthocyanins. Phytochemistry 53:659–665
Walker AR, Lee E, Robinson SP (2006) Two new grape cultivars, bud sports of Cabernet Sauvignon bearing pale-coloured berries, are the result of deletion of two regulatory genes of the berry colour locus. Plant Mol Biol 62(4–5):623–635. https://doi.org/10.1007/s11103-006-9043-9
Yakushiji H, Kobayashi S, Goto-Yamamoto N, Tae Jeong S, Sueta T, Mitani N, Azuma A (2014) A skin color mutation of grapevine, from black-skinned Pinot Noir to white-skinned Pinot Blanc, is caused by deletion of the functional VvmybA1 allele. Biosci Biotechnol Biochem 70(6):1506–1508. https://doi.org/10.1271/bbb.50647
Zhang P, Wen PF, Wan SB, Wang W, Pan QH, Zhan JC, Huang WD (2008) Molecular cloning of dihydroflavonol 4-reductase gene from grape berry and preparation of an anti-DFR polyclonal antibody. Vitis 47:141–145
Zheng Y, Tian L, Liu H, Pan Q, Zhan J, Huang W (2009) Sugars induce anthocyanin accumulation and flavanone 3-hydroxylase expression in grape berries. Plant Growth Regul 58(3):251–260. https://doi.org/10.1007/s10725-009-9373-0
Acknowledgements
This research was supported partly by the National Key R&D Program of China (2018YFD1000200) and was conducted as part of the LIA INNOGRAPE International Associated Laboratory. We thank Jean-Pierre Petit for assistance in preparing plant materials and Christel Renaud for assistance in biochemical analysis.
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Kong, J., Wu, J., Guan, L. et al. Metabolite analysis reveals distinct spatio-temporal accumulation of anthocyanins in two teinturier variants of cv. ‘Gamay’ grapevines (Vitis vinifera L.). Planta 253, 84 (2021). https://doi.org/10.1007/s00425-021-03613-4
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DOI: https://doi.org/10.1007/s00425-021-03613-4