Abstract
Key message
Wild and loss-of-function alleles of the 5 - O - glucosyltransferase gene responsible for synthesis of diglucoside anthocyanins in Vitis were characterized. The information aids marker development for tracking this gene in grape breeding.
Abstract
Anthocyanins in red grapes are present in two glycosylation states: monoglucoside (3-O-glucoside) and diglucoside (3, 5-di-O-glucoside). While monoglucoside anthocyanins are present in all pigmented grapes, diglucoside anthocyanins are rarely found in the cultivated grape species Vitis vinifera. Biochemically 3-O-glucoside anthocyanins can be converted into 3,5-di-O-glucoside anthocyanins by a 5-O-glucosyltransferase. In this study, we surveyed allelic variation of the 5-O-glucosyltransferase gene (5GT) in 70 V. vinifera ssp. vinifera cultivars, 52 V. vinifera ssp. sylvestris accessions, 23 Vitis hybrid grapes, and 22 accessions of seven other Vitis species. Eighteen 5GT alleles with apparent loss-of-function mutations, including seven premature stop codon mutations and six frameshift indel mutations, were discovered in V. vinifera, but not in the other Vitis species. A total of 36 5GT alleles without apparent loss-of-function mutations (W-type) were identified. These W-type alleles were predominantly present in wild Vitis species, although a few of them were also found in some V. vinifera accessions. We further evaluated some of these 5GT alleles in producing diglucoside anthocyanins by analyzing the content of diglucoside anthocyanins in a set of representative V. vinifera cultivars. Through haplotype network analysis we revealed that V. vinifera ssp. vinifera and its wild progenitor V. vinifera ssp. sylvestris shared many loss-of-function 5GT alleles and extensive divergence of the 5GT alleles was evident within V. vinifera. This work advances our understanding of the genetic diversity of 5GT and provides a molecular basis for future marker-assisted selection for improving this important wine quality trait.
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References
Anderson DW, Julian EA, Kepner RE, Webb AD (1970) Chromatographic investigation of anthocyanin pigments in Vitis cinerea. Phytochemistry 9:1569–1578
Balík J, Kumšta M, Rop O (2013) Comparison of anthocyanins present in grapes of Vitis vinifera L. varieties and interspecific hybrids grown in the Czech Republic. Chem Pap 67:1285–1292
Ballinger WE, Maness EP, Nesbitt WB, Carroll DE (1973) Anthocyanins of black grapes of 10 clones of Vitis rotundifolia, Michx. J Food Sci 38:909–910
Bishop PD, Nagel CW (1984) Characterization of the condensation product of malvidin 3,5-diglucoside and catechin. J Agr Food Chem 32:1022–1026
De la Cruz AA, Hilbert G, Riviere C, Mengin V, Ollat N, Bordenave L, Decroocq S, Delaunay JC, Delrot S, Merillon JM, Monti JP, Gomes E, Richard T (2012) Anthocyanin identification and composition of wild Vitis spp. accessions by using LC-MS and LC-NMR. Anal Chim Acta 732:145–152
De Rosso M, Tonidandel L, Larcher R, Nicolini G, Ruggeri V, Dalla Vedova A, De Marchi F, Gardiman M, Flamini R (2012) Study of anthocyanic profiles of twenty-one hybrid grape varieties by liquid chromatography and precursor-ion mass spectrometry. Anal Chim Acta 732:120–129
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Eibach R, Töpher R (2003) Success in resistance breeding: “REGENT” and its steps into the market. Acta Hort (ISHS) 603:687–691
Flamini R, Tomasi D (2000) The anthocyanin content in berries of the hybrid grape cultivars Clinton and Isabella. Vitis 39:79–81
Ford CM, Boss PK, Hoj PB (1998) Cloning and characterization of Vitis vinifera UDP-glucose : flavonoid 3-O-glucosyltransferase, a homologue of the enzyme encoded by the maize Bronze-1 locus that may primarily serve to glucosylate anthocyanidins in vivo. J Biol Chem 273:9224–9233
Garcia-Viguera C, Bridle P (1999) Influence of structure on colour stability of anthocyanins and flavylium salts with ascorbic acid. Food Chem 64:21–26
Hausmann L, Neumann K, Eibach R, Zyprian E, Töpfer R (2009) Development of a molecular marker for an anthocyanin 5-O-glucosyl transferase homologous gene of Vitis ssp. correlated with anthocyanin 3,5-diglucoside formation in berry skin. Acta Hort (ISHS) 827:457–460
Hausmann L, Eibach R, Toepfer R (2010) Alleles of anthocyanin 5-glucosyltransferase of Vitis vinifera are non-functional. Austr J Grape Wine Res 16(Suppl 1):A15
Huang ZL, Wang BW, Williams P, Pace RD (2009) Identification of anthocyanins in muscadine grapes with HPLC-ESI-MS. Lwt-Food Sci Technol 42:819–824
Janvary L, Hoffmann T, Pfeiffer J, Hausmann L, Topfer R, Fischer TC, Schwab W (2009) A double mutation in the anthocyanin 5-O-glucosyltransferase gene disrupts enzymatic activity in Vitis vinifera L. J Agr Food Chem 57:3512–3518
Kim M, Yoon SH, Jung M, Choe E (2010) Stability of meoru (Vitis coignetiea) anthocyanins under photochemically produced singlet oxygen by riboflavin. New Biotechnol 27:435–439
Li Y, Ma R, Xu Z, Wang J, Chen T, Chen F, Wang Z (2013) Identification and quantification of anthocyanins in Kyoho grape juice-making pomace, Cabernet Sauvignon grape winemaking pomace and their fresh skin. J Sci Food Agric 93:1404–1411
Liang ZC, Owens CL, Zhong GY, Cheng LL (2011) Polyphenolic profiles detected in the ripe berries of Vitis vinifera germplasm. Food Chem 129:940–950
Liang ZC, Yang YZ, Cheng LL, Zhong GY (2012) Polyphenolic composition and content in the ripe berries of wild Vitis species. Food Chem 132:730–738
Liang ZC, Yang YZ, Cheng LL, Zhong GY (2013) Characterization of polyphenolic metabolites in grape hybrids. Vitis 52:51–59
Lijavetzky D, Cabezas JA, Ibanez A, Rodriguez V, Martinez-Zapater JM (2007) High throughput SNP discovery and genotyping in grapevine (Vitis vinifera L.) by combining a re-sequencing approach and SNPlex technology. BMC Genom 8:424
Mazza G (1995) Anthocyanins in grapes and grape products. Crit Rev Food Sci 35:341–371
Mazza G, Brouillard R (1987) Color stability and structural transformations of cyanidin 3,5-diglucoside and four 3-deoxyanthocyanins in aqueous solutions. J Agr Food Chem 35:422–426
McGovern PE (2003) Ancient wine: the search for the origins of viniculture. Princeton University Press, Princeton
Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, Aradhya MK, Prins B, Reynolds A, Chia JM, Ware D, Bustamante CD, Buckler ES (2011) Genetic structure and domestication history of the grape. Proc Natl Acad Sci USA 108:3530–3535
Okamoto G (2007) Poor berry set in tetraploid grapes-causes and improvement of vineyard practices. J ASEV Jpn 18:94–106
Picariello G, Ferranti P, Chianese L, Addeo F (2012) Differentiation of Vitis vinifera L. and hybrid red grapes by matrix-assisted laser desorption/ionization mass spectrometry analysis of berry skin anthocyanins. J Agr Food Chem 60:4559–4566
Picariello G, Ferranti P, Garro G, Manganiello G, Chianese L, Coppola R, Addeo F (2014) Profiling of anthocyanins for the taxonomic assessment of ancient purebred V. vinifera red grape varieties. Food Chem 146:15–22
Revilla E, Carrasco D, Benito A, Arroyo-Garcia R (2010) Anthocyanin composition of several wild grape accessions. Am J Enol Viticult 61:536–543
Riahi L, Zoghlami N, Dereeper A, Laucou V, Mliki A, This P (2013) Single nucleotide polymorphism and haplotype diversity of the gene NAC4 in grapevine. Ind Crop Prod 43:718–724
Robinson WB, Weirs LD, Bertino JJ, Mattick LR (1966) The relation of anthocyanin composition to color stability of New York state wines. Am J Enol Vitic 17:178–184
Sandhu AK, Gu LW (2010) Antioxidant capacity, phenolic content, and profiling of phenolic compounds in the seeds, skin, and pulp of Vitis rotundifolia (Muscadine grapes) as determined by HPLC-DAD-ESI-MSn. J Agr Food Chem 58:4681–4692
Sims CA, Morris JR (1985) A comparison of the color components and color stability of red wine from Noble and Cabernet Sauvignon at various pH levels. Am J Enol Viticult 36:181–184
Sims CA, Morris JR (1986) Effects of acetaldehyde and tannins on the color and chemical age of red muscadine (Vitis rotundifolia) wine. Am J Enol Viticult 37:163–165
Templeton AR, Crandall KA, Sing CF (1992) A cladistic-analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA-sequence data.III. cladogram estimation. Genetics 132:619–633
This P, Lacombe T, Thomas MR (2006) Historical origins and genetic diversity of wine grapes. Trends Genet 22:511–519
Vanburen JP, Bertino JJ, Robinson WB (1968) Stability of wine anthocyanins on exposure to heat and light. Am J Enol Viticult 19:147–154
Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, FitzGerald LM et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326
Wang J, De Luca V (2005) The biosynthesis and regulation of biosynthesis of Concord grape fruit esters, including ‘foxy’ methylanthranilate. Plant J 44:606–619
Wu X, Prior RL (2005) Systematic identification and characterization of anthocyanins by HPLC-ESI-MS/MS in common foods in the United States: fruits and berries. J Agr Food Chem 53:2589–2599
Yamazaki M, Gong Z, Fukuchi-Mizutani M, Fukui Y, Tanaka Y, Kusumi T, Saito K (1999) Molecular cloning and biochemical characterization of a novel anthocyanin 5-O-glucosyltransferase by mRNA differential display for plant forms regarding anthocyanin. J Biol Chem 274:7405–7411
Yamazaki M, Yamagishi E, Gong ZZ, Fukuchi-Mizutani M, Fukui Y, Tanaka Y, Kusumi T, Yamaguchi M, Saito K (2002) Two flavonoid glucosyltransferases from Petunia hybrida: molecular cloning, biochemical properties and developmentally regulated expression. Plant Mol Biol 48:401–411
You Q, Chen F, Wang X, Sharp JL, You YR (2012) Analysis of phenolic composition of Noble muscadine (Vitis rotundifolia) by HPLC-MS and the relationship to its antioxidant capacity. J Food Sci 77:C1115–C1123
Zhao Q, Duan CQ, Wang J (2010) Anthocyanins profile of grape berries of Vitis amurensis, its hybrids and their wines. Int J Mol Sci 11:2212–2228
Zhu L, Zhang YL, Lu J (2012) Phenolic contents and compositions in skins of red wine grape cultivars among various genetic backgrounds and originations. Int J Mol Sci 13:3492–3510
Acknowledgments
We wish to thank Andy Humiston of Department of Horticulture, Cornell University for providing his assistance in HPLC analysis of anthocyanins and Thomas Chao, Dawn Dellefave and Bill Srmack of USDA-ARS, Plant Genetic Resources Unit for their assistance in collecting tissue samples from the USDA-ARS Geneva Vitis Clonal Repository. USDA-ARS is an equal opportunity provider and employer. The use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable. This project was funded by the United States Department of Agriculture, Agricultural Research Service, CRIS Project Number 1910-21000-020-00D.
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Communicated by Reinhard Toepfer.
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Yang, Y., Labate, J.A., Liang, Z. et al. Multiple loss-of-function 5-O-glucosyltransferase alleles revealed in Vitis vinifera, but not in other Vitis species. Theor Appl Genet 127, 2433–2451 (2014). https://doi.org/10.1007/s00122-014-2388-6
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DOI: https://doi.org/10.1007/s00122-014-2388-6