Skip to main content
SpringerLink
Log in

Exploring quantitative trait loci for anthocyanin content in interspecific hybrid grape (Vitis labruscana × Vitis vinifera)

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Anthocyanins affect the coloration of grape berry skin, which is an important determinant for consumer choice and grape marketability. Molecular mechanisms for anthocyanin accumulation in grape skin have been intensively studied. In Vitis vinifera, two adjacent MYB transcriptional factors, VvMybA1 and VvMybA2, regulate anthocyanin biosynthesis, and these genes can be regarded as a MYB haplotype. Interspecific hybrid grape (Vitis labruscana × V. vinifera) is particularly valuable in wet climate regions, yet few studies on anthocyanin accumulation in this hybrid have been published. Using 98 F1 individuals from a V. labruscana × V. vinifera cross, we constructed the parental and consensus linkage maps with simple sequence repeat markers, and performed quantitative trait locus (QTL) analysis of anthocyanin content. Distribution of anthocyanin content showed continuous variation, which was mainly due to the effect of genotypes. We detected QTLs for anthocyanin content in linkage groups 2 (A2-QTL1 = MYB haplotype), 8 (A8-QTL2) and 14 (A14-QTL3). These results suggest that A8-QTL2 and A14-QTL could be novel loci that affect anthocyanin content in berry skin.

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

  • Alleweldt G, Possingham JV (1988) Progress in grapevine breeding. Theor Appl Genet 75:669–673

    Article  Google Scholar 

  • Alleweldt G, Spiegel-Roy P, Reisch B (1990) Grapes (Vitis) In: Moore JN, Ballington JR (eds) Genetic resources of temperate fruit and nuts crops. Acta Hort 290, pp 291–327

  • 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  CAS  PubMed  Google Scholar 

  • Azuma A, Udo Y, Sato A, Mitani N, Kono A, Ban Y, Yakushiji H, Koshita Y, Kobayashi S (2011) 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

    Article  PubMed  Google Scholar 

  • Ballea E (1975) Inheritance of some characters and traits in F1 hybrid progeny from crosses of Coarncă neagră with various male parents. Vitic Sivini 46:31–44

    Google Scholar 

  • Barritt BH, Einset J (1969) The inheritance of three major fruit colors in grapes. J Am Soc Hortic Sci 94:87–89

    Google Scholar 

  • Bayo-Canha A, Fernández-Fernández JI, Martínez-Cutillas A, Ruiz-García L (2012) Phenotypic segregation and relationships of agronomic traits in Monastrell x Syrah wine grape progeny. Euphytica 186:393–407

    Article  CAS  Google Scholar 

  • Beavis WD (1998) QTL analyses: power, precision, and accuracy. In: Paterson AH (ed) Molecular dissection of complex traits. CRC Press LLC, New York, pp 145–162

    Google Scholar 

  • Campbell RC (1974) Statistics for biologists, 2nd edn. Baifukan, Tokyo

    Google Scholar 

  • Cardoso S, Lau W, Eiras Dias J, Fevereiro P, Maniatis N (2012) A candidate-gene association study for berry colour and anthocyanin content in Vitis vinifera L. PLoS ONE 7:e46021

    Article  PubMed Central  PubMed  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  CAS  PubMed  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed Central  PubMed  Google Scholar 

  • Costantini L, Battilana J, Lamaj F, Fanizza G, Grando MS (2008) Berry and phenology-related traits in grapevine (Vitis vinifera L.): From Quantitative Trait Loci to underlying genes. BMC Plant Biol 8:38

    Article  PubMed Central  PubMed  Google Scholar 

  • Doligez A, Bouquet A, Danglot Y, Lahogue F, Riaz S, Meredith CP, Edwards KJ, This P (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  CAS  PubMed  Google Scholar 

  • Doligez A, Adam-Blondon AF, Cipriani G, Di Gaspero G, Laucou V, Merdinoglu D, Meredith CP, Riaz S, Roux C, This P (2006) An integrated SSR map of grapevine based on five mapping populations. Theor Appl Genet 113:369–382

    Article  CAS  PubMed  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  CAS  PubMed Central  PubMed  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  CAS  PubMed  Google Scholar 

  • Goldy RG (1989) Pigment quantity and quality characteristics of some native Vitis rotudifolia Michx. Am J Enol Vitic 40:253–258

    CAS  Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudotestcross: mapping strategy and RAPD markers. Genetics 137:1121–1137

    CAS  PubMed Central  PubMed  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 

  • Jackson D, Culianez-Maciab F, Prescott AG, Roberts K, Martin C (1991) Expression Patterns of myb Genes from Antirrhinum Flowers. Plant Cell 3:115–125

    Article  CAS  PubMed Central  PubMed  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, Bruyère 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, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quétier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liang Z, Yang C, Jun Yang J, Wu B, Wang L, Cheng J, Li S (2009) Inheritance of anthocyanins in berries of Vitis vinifera grapes. Euphytica 167:113–125

    Article  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 

  • Luo SL, He PC (2004) The inheritances of fruit skin and must colors in a series of interspecific and intraspecific crosses between Vitis vinifera and the wild grape species native to China. Sci Hortic 99:29–40

    Article  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 Central  PubMed  Google Scholar 

  • Matus JT, Poupin MJ, Cañón P, Bordeu E, Alcalde JA, Arce-Johnson P (2010) Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.). Plant Mol Biol 72:607–620

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Nishio S, Yamada M, Sawamura Y, Takada N, Saito T (2011) Environmental variance components of fruit ripening date as used in both phenotypic and marker-assisted selection in Japanese pear breeding. HortScience 46:1540–1544

    Google Scholar 

  • Park KS, Yun HK, Bouk RJS, Sang K, Lee J, Jae H (2003) Inheritance of stenospermocarpic seedlessness in grapes (Vitis spp.). J Korean Soc Hortic Sci 44:675–677

    Google Scholar 

  • R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL: http://www.R-project.org/

  • Reisch BI, Pratt C (1996) Grapes. In: Janick J, Moore JN (eds) Fruit breeding. Wiley, New York, pp 297–369

    Google Scholar 

  • Sandhu AS (1988) Inheritance of berry color in grapes (Vitis vinifera). J Res Punjab Agric Univ 25:37–39

    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 

  • Spiegel-Roy P, Assaf R (1980) Inheritance of some characters in progeny of Vitis vinifera from crosses with Dabouki and Alphonse Lavallee. In: Proceedings of the third intenational symposium on grape breeding. 15–18 June 1980, Davis, CA. Department of Viticulture and Enology, University of California, Davis, pp 210–219

  • Terakami S, Kimura T, Nishitani C, Sawamura Y, Saito T, Hirabayashi T, Yamamoto T (2009) Genetic linkage map of the Japanese pear ‘Housui’ identifying three homozygous genomic regions. J Jpn Soc Hort Sci 78:417–424

    Article  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 

  • Ukai Y (2000) Genetic analysis at the genomic level: Map and QTL. University of Tokyo Press, Tokyo, Japan

    Google Scholar 

  • Van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V. Wageningen, Netherlands

  • Van Ooijen JW (2009) MapQTL® 6, Software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma B.V. Wageningen, Netherlands

  • 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, Soloviev V, Fawcett JA, Sterck L, Grando MS, 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 2:e1326

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Yamada M, Yamane H, Yoshinaga K, Ukai Y (1993) Optimal spatial and temporal measurement repetition for selection in Japanese persimmon breeding. HortScience 28:838–841

    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 

Download references

Acknowledgments

We thank Drs Toshiya Yamamoto and Shingo Terakami (NIFTS) for their valuable suggestions regarding the construction of linkage maps. We also thank Tamami Nakasumi and Junko Azuma (NIFTS) for technical assistance. This work was supported in part by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Development of mitigation and adaptation techniques to global warming in the sectors of agriculture, forestry, and fisheries, C-3-2030).

Author information

Authors and Affiliations

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

    Yusuke Ban, Akihiko Sato, Akifumi Azuma, Atsushi Kono & Shozo Kobayashi

  2. National Agriculture and Food Research Organization Institute of Fruit Tree Science, 2-1 Fujimoto, Tsukuba, Ibaraki, 305-8605, Japan

    Nobuhito Mitani

  3. National Agriculture and Food Research Organization Agricultural Research Center, 3-1-1 Kannondai, Tsukuba, Ibaraki, 305-8666, Japan

    Takeshi Hayashi

Authors
  1. Yusuke Ban
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nobuhito Mitani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takeshi Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akihiko Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Akifumi Azuma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Atsushi Kono
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shozo Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yusuke Ban.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ban, Y., Mitani, N., Hayashi, T. et al. Exploring quantitative trait loci for anthocyanin content in interspecific hybrid grape (Vitis labruscana × Vitis vinifera). Euphytica 198, 101–114 (2014). https://doi.org/10.1007/s10681-014-1087-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-014-1087-3

Keywords

Search

Navigation