Skip to main content
SpringerLink
Log in

Haplotype composition at the color locus is a major genetic determinant of skin color variation in Vitis ×labruscana grapes

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Skin color is one of the most important fruit traits in grape, and has become greatly diversified due to hybridization and human selection. Many studies concerning the genetic control of grape color in European species (Vitis vinifera L.), especially the role of MYB-related genes, have been reported. On the other hand, there have been few studies of the MYB-related genes in grapes belonging to V. ×labruscana L.H. Bailey, a subgroup of grapes that originated from the hybridization of V. labrusca with V. vinifera. In the present study, we found a novel functional haplotype, HapE2 (consisting of the genes VlMYBA2 and VlMYBA1–3), in diploid V. ×labruscana. Moreover, we developed a method to determine the haplotype compositions of tetraploid grapes by means of quantitative real-time PCR, and investigated the relationship between haplotype composition and skin color. The color locus in V. ×labruscana grapes usually consists of functional haplotypes (HapE1 and/or HapE2), and non-functional haplotype HapA. The number of functional haplotypes in the genome was found to be correlated with the level of anthocyanin in the skin. Anthocyanin contents of grapes that contained HapE2 were significantly higher than those containing HapE1. These results suggest that the number and kind of functional haplotypes at the color locus are the major genetic factors that determine skin color variation. These findings provide new knowledge about the unique genetic control of color in V. ×labruscana grapes, and should contribute to development of new cultivars that have the desired color and anthocyanin content.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akagi T, Kanzaki S, Gao M, Tao R, Parfitt DE, Yonemori K (2009) Quantitative real-time PCR to determine allele number for the astringency locus by analysis of a linked marker in Diospyros kaki Thunb. Tree Genet Gen 5:483–492

    Article  Google Scholar 

  • Azuma A, Kobayashi S, Yakushiji H, Yamada M, Mitani N, Sato A (2007) VvmybA1 genotype determines grape skin color. Vitis 46:154–155

    CAS  Google Scholar 

  • Azuma A, Kobayashi S, Mitani N, Shiraishi M, Yamada M, Ueno T, Kono A, Yakushiji H, Koshita Y (2008) Genomic and genetic analysis of Myb-related genes that regulate anthocyanin biosynthesis in grape berry skin. Theor Appl Genet 117:1009–1019

    Article  PubMed  CAS  Google Scholar 

  • Azuma A, Kobayashi S, Goto-Yamamoto N, Shiraishi M, Mitani N, Yakushiji H, Koshita Y (2009) Color recovery in berries of grape (Vitis vinifera L.) ‘Benitaka’, a bud sport of ‘Italia’, is caused by a novel allele at the VvmybA1 locus. Plant Sci 176:470–478

    Article  CAS  Google Scholar 

  • Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143:1347–1361

    Article  PubMed  CAS  Google Scholar 

  • Castellarin SD, Matthews MA, Gaspere GD, Gambetta GA (2007) Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227:101–112

    Article  PubMed  CAS  Google Scholar 

  • Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Mérillon JM, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140:499–511

    Article  PubMed  CAS  Google Scholar 

  • Deluc L, Bogs J, Walker AR, Ferrier T, Decendit A, Merillon JM, Robinson SP, Barrieu F (2008) The transcription factor VvMYB5b contributes to the regulation of anthocyanin and proanthocyanin biosynthesis in developing grape berries. Plant Physiol 147:2041–2053

    Article  PubMed  CAS  Google Scholar 

  • Doligez A, Bouquet A, Danglot Y, Lahogue F, Riaz S, Meredith CP, Edwards KJ (2002) Genetic mapping of grapevine (Vitis vinifera L.) applied to the detection of QTLs for seedlessness and berry weight. Theor Appl Genet 105:780–795

    Article  PubMed  CAS  Google Scholar 

  • Einset J, Pratt C (1975) Grapes. In: Janick J, Moore JN (eds) Advances in fruit breeding. Purdue University Press, West Lafayette, pp 130–153

    Google Scholar 

  • Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Topfer R, Zyprian EM (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515

    Article  PubMed  CAS  Google Scholar 

  • 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 183:1127–1139

    Article  PubMed  CAS  Google Scholar 

  • Fournier-Level A, Lacombe T, Le Cunff L, Boursiquot JM, This P (2010) Evolution of the VvMybA gene family, the major determinant of berry colour in cultivated grapevine (Vitis vinifera L.). Heredity 104:351–362

    Article  PubMed  CAS  Google Scholar 

  • Giannetto S, Velasco R, Troggio M, Malacarne G, Storchi P, Cancellier S, De Nardi B, Crespan M (2008) A PCR-based diagnostic tool for distinguishing grape skin color mutants. Plant Sci 175:402–409

    Article  CAS  Google Scholar 

  • Hedrick UP (1908) The grapes of New York. Albany J B Company, State Printers

    Google Scholar 

  • Hedrick UP (1925) Systematic pomology. Macmillan, New York

    Google Scholar 

  • Henry IM, Dilkes BP, Comai L (2006) Molecular karyotyping and aneuploidy detection in Arabidopsis thaliana using quantitative fluorescent polymerase chain reaction. Plant J 48:307–319

    Article  PubMed  CAS  Google Scholar 

  • Hiratsuka S, Onodera H, Kawai Y, Kubo T, Itoh H, Wada R (2001) ABA and sugar effects on anthocyanin formation in grape berry cultured in vitro. Sci Hort 90:121–130

    Article  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  PubMed  CAS  Google Scholar 

  • Jeong ST, Goto-Yamamoto N, Kobayashi S, Esaka M (2004) Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci 167:247–252

    Article  CAS  Google Scholar 

  • Kataoka I, Kubo Y, Sugiura A, Tomana T (1984) effects of temperature, cluster shading and some growth regulators on l-phenylalanine ammonia-lyase activity and anthocyanin accumulation on black grapes. Mem Coll Agric Kyoto Univ 124:35–44

    CAS  Google Scholar 

  • Kataoka I, Sugiyama A, Beppu K (2003) Role of ultraviolet radiation in accumulation of anthocyanin in berries of ‘Gros Colman’ grapes (Vitis vinifera L.). J Jpn Soc Hort Sci 72:1–6

    Article  CAS  Google Scholar 

  • Kliewer WM, Torres RE (1972) Effect of controlled day and night temperatures on grape coloration. Am J Enol Vitic 23:71–77

    Google Scholar 

  • Kobayashi S, Ishimaru M, Hiraoka K, Honda C (2002) Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215:924–933

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982

    Article  PubMed  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2005) Association of VvmybA1 gene expression with anthocyanin production in grape (Vitis vinifera) skin-color mutants. J Jpn Soc Hort Sci 74:196–203

    Article  CAS  Google Scholar 

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids; a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242

    Article  PubMed  CAS  Google Scholar 

  • Lijavetzky D, Ruiz-Garcia L, Cabezas JA, de Andres MT, Bravo G, Ibanez A, Carreno J, Cabello F, Ibanez J, Martinez-Zapater JM (2006) Molecular genetics of berry colour variation in table grape. Mol Gen Genom 276:427–435

    Article  CAS  Google Scholar 

  • Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83

    Article  PubMed  Google Scholar 

  • Matus JT, Loyola R, Vega A, Peña-Neira A, Bordeu E, Arce-Johnson P, Alcalde JA (2009) Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera. J Exp Bot 60:853–867

    Article  PubMed  CAS  Google Scholar 

  • Mitani N, Azuma A, Fukai E, Hirochika H, Kobayashi S (2009) A retrotransposon-inserted VvmybA1a allele has been spread among cultivars of Vitis vinifera but not in North American and East Asian Vitis species. Vitis 48:55–56

    Google Scholar 

  • Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58:1935–1945

    Article  PubMed  CAS  Google Scholar 

  • Salmaso M, Malacarne G, Troggio M, Faes G, Stefanini M, Grando MS, Velasco R (2008) A grapevine (Vitis vinifera L.) genetic map integrating the position of 139 expressed genes. Theor Appl Genet 116:1129–1143

    Article  PubMed  CAS  Google Scholar 

  • Shiraishi M, Yamada M, Mitani N, Ueno T (2007) A rapid determination method for anthocyanin profiling in grape genetic resources. J Jpn Soc Hort Sci 76:28–35

    Article  CAS  Google Scholar 

  • Snyder E (1937) Grape development and improvement. In: Yearbook of agriculture 1937. Washington, DC, pp 631–664

  • Terrier N, Torregrosa L, Ageorges A, Vialet S, Verriès C, Cheynier V, Romieu C (2009) Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol 149:1028–1041

    Article  PubMed  CAS  Google Scholar 

  • This P, Lacombe T, Cadle-Davidson M, Owens CL (2007) Wine grape (Vitis vinifera L.) color associates with allelic variation in the domestication gene VvmybA1. Theor Appl Genet 114:723–730

    Article  PubMed  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Demattè L, Mraz A, Battilana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326

    Article  PubMed  Google Scholar 

  • 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 62:623–635

    Article  PubMed  CAS  Google Scholar 

  • Walker AR, Lee E, Bogs J, McDavid DAJ, Thomas MR, Robinson SP (2007) White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J 49:772–785

    Article  PubMed  CAS  Google Scholar 

  • Winkler AJ, Cook JA, Kliewer WM, Lider LA (1974) General viticulture. University of California Press, Berkley

    Google Scholar 

  • Yakushiji H, Kobayashi S, Goto-Yamamoto N, Jeong ST, Sueta T, Mitani N, Azuma A (2006) A skin color mutation of grapevine, from black-skinned ‘Pinot Noir’ to white-skinned ‘Pinot Blanc’ is caused by the deletion of the functional VvmybA1 allele. Biosci Biotechnol Biochem 70:1506–1508

    Article  PubMed  CAS  Google Scholar 

  • Yamane T, Jeong ST, Goto-Yamamoto N, Koshita Y, Kobayashi S (2006) Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am J Enol Vitic 57:54–59

    CAS  Google Scholar 

  • 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 58:251–260

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported in part by a grant from the research program “Development of technology for impacts, mitigation and adaptation of climate change” provided by the Ministry of Agriculture, Forestry and Fisheries, Japan.

Author information

Authors and Affiliations

  1. Grape and Persimmon Research Station, National Institute of Fruit Tree Science, 301-2 Akitsu, Higashi-Hiroshima, Hiroshima, 739-2494, Japan

    Akifumi Azuma, Akihiko Sato, Nobuhito Mitani, Atsushi Kono, Yusuke Ban, Hiroshi Yakushiji, Yoshiko Koshita & Shozo Kobayashi

  2. Yamanashi Fruit Tree Experiment Station, 1204 Ezohara, Yamanashi, 405-0043, Japan

    Yukinobu Udo

Authors
  1. Akifumi Azuma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yukinobu Udo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akihiko Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nobuhito Mitani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Atsushi Kono
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yusuke Ban
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hiroshi Yakushiji
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yoshiko Koshita
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shozo Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akifumi Azuma.

Additional information

Communicated by Y. Xue.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Azuma, A., Udo, Y., Sato, A. et al. Haplotype composition at the color locus is a major genetic determinant of skin color variation in Vitis ×labruscana grapes. Theor Appl Genet 122, 1427–1438 (2011). https://doi.org/10.1007/s00122-011-1542-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-011-1542-7

Keywords

Search

Navigation