Skip to main content
Log in

Linkage disequilibrium in cultivated grapevine, Vitis vinifera L

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

Abstract

We present here the first study of linkage disequilibrium (LD) in cultivated grapevine, Vitis vinifera L. subsp. vinifera (sativa), an outcrossing highly heterozygous perennial species. Our goal was to characterize the amount and pattern of LD at the scale of a few centiMorgans (cM) between 38 microsatellite loci located on five linkage groups, in order to assess its origin and potential applications. We used a core collection of 141 cultivars representing the diversity of the cultivated compartment. LD was evaluated with both independence tests and multilocus r 2, both on raw genotypic and reconstructed haplotypic data. Significant genotypic LD was found only within linkage groups, extending up to 16.8 cM. It appeared not to be influenced by the weak structure of the sample and seemed to be mainly of haplotypic origin. Significant haplotypic LD was found over 30 cM. Both genotypic and haplotypic r 2 values declined to around 0.1 within 5–10 cM, suggesting a rather narrow genetic base of the cultivated compartment and limited recombination since domestication events. These first results open up a few application opportunities for association mapping of QTLs and marker assisted selection.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adam-Blondon AF, Roux C, Claux D, Butterlin G, Merdinoglu D, This P (2004) Mapping 245 SSR markers on the Vitis vinifera genome: a tool for grape genetics. Theor Appl Genet 109:1017–1027

    Article  PubMed  CAS  Google Scholar 

  • Adam-Blondon AF, Bernole A, Faes G, Lamoureux D, Pateyron S, Grando MS, Caboche M, Velasco R, Chalhoub B (2005) Construction and characterization of BAC libraries from major grapevine cultivars. Theor Appl Genet 110:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Aradhya MK, Dangl GS, Prins BH, Boursiquot JM, Walker MA, Meredith CP, Simon CJ (2003) Genetic structure and differentiation in cultivated grape, Vitis vinifera L. Genet Res 81:179–192

    Article  PubMed  CAS  Google Scholar 

  • Arroyo-Garcia R, Lefort F, de Andrés MT, Ibañez J, Borrego J, Jouve N, Cabello F, Martinez-Zapater JM (2002) Chloroplast microsatellite polymorphisms in Vitis species. Genome 45:1142–1149

    Article  PubMed  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2002) GENETIX 4.04, logiciel sous Windows pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France

  • Bowers J, Boursiquot JM, This P, Chu K, Johansson H, Meredith C (1999) Historical genetics: the parentage of Chardonnay, Gamay, and other wine grapes of Northeastern France. Science 285:1562–1565

    Article  PubMed  CAS  Google Scholar 

  • Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Nat Acad Sci USA 101:15255–15260

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Farnir F, Coppieters W, Arranz JJ, Berzi P, Cambisano N, Grisart B, Karim L, Marcq F, Moreau L, Mni M, Nezer C, Simon P, Vanmanshoven P, Wagenaar D, Georges M (2000) Extensive genome-wide linkage disequilibrium in cattle. Genome Res 10:220–227

    Article  PubMed  CAS  Google Scholar 

  • Garris AJ, Mccouch SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165:759–769

    PubMed  Google Scholar 

  • Grassi F, Labra M, Imazio S, Spada A, Sgorbati S, Scienza A, Sala F (2003) Evidence of a secondary grapevine domestication centre detected by SSR analysis. Theor Appl Genet 107:1315–1320

    Article  PubMed  CAS  Google Scholar 

  • Gouesnard B, Bataillon TM, Decoux G, Rozale C, Schoen DJ, David JL (2001) Mstrat: an algorithm for building germplasm core collections by maximizing allelic or phenotypic richness. J Hered 92:93–94

    Article  PubMed  CAS  Google Scholar 

  • Hamblin MT, Mitchell SE, White GM, Gallego J, Kukatla R, Wing RA, Paterson AH, Kresovich S (2004) Comparative population genetics of the panicoid grasses: sequence polymorphism, linkage disequilibrium and selection in a diverse sample of Sorghum bicolor. Genetics 167:471–483

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW (1987) Gametic disequilibrium measures: proceed with caution. Genetics 117:331–341

    PubMed  CAS  Google Scholar 

  • Jannoo N, Grivet L, Dookun A, D’hont A, Glaszmann JC (1999) Linkage disequilibrium among modern sugarcane cultivars. Theor Appl Genet 99:1053–1060

    Article  CAS  Google Scholar 

  • Jorde LB (2000) Linkage disequilibrium and the search for complex disease genes. Genome Res 10:1435–1444

    Article  PubMed  CAS  Google Scholar 

  • Jung M, Ching A, Bhattramakki D, Dolan M, Tingey S, Morgante M, Rafalski A (2004) Linkage disequilibrium and sequence diversity in a 500-kbp region around the adh1 locus in elite maize germplasm. Theor Appl Genet 109:681–689

    Article  PubMed  CAS  Google Scholar 

  • Kraakman ATW, Niks RE, Van den Berg PMMM, Stam P, Van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446

    Article  PubMed  CAS  Google Scholar 

  • Kruglyak L (1999) Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nat Genet 22:139–144

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Echt C, Wilcox PL, Richardson TE (2004) Testing for linkage disequilibrium in the New Zealand radiata pine breeding population. Theor Appl Genet 108:292–298

    Article  PubMed  CAS  Google Scholar 

  • Lewis PO, Zaykin D (2002) GDA 1.1. The University of Connecticut

  • Lewontin RC (1988) On measures of gametic disequilibrium. Genetics 120:849–852

    PubMed  CAS  Google Scholar 

  • Maccaferri M, Sanguineti MC, Noli E, Tuberosa R (2005) Population structure and long-range linkage disequilibrium in a durum wheat elite collection. Mol Breed 15:271–289

    Article  CAS  Google Scholar 

  • MacRae AF, McEwan JC, Dodds KG, Wilson T, Crawford AM, Slate J (2002) Linkage disequilibrium in domestic sheep. Genetics 160:1113–1122

    Google Scholar 

  • Mohlke KL, Lange EM, Valle TT, Ghosh S, Magnuson V L, Silander K, Watanabe RM, Chines PS, Bergman RN, Tuomilehto A, Collins FS, Boehnke M (2001) Linkage disequilibrium between microsatellite markers extends beyond 1 cM on chromosome 20 in Finns. Genome Res 11:1221–1226

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1978) Eestimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Nei M, Li WH (1973) Linkage disequilibrium in subdivided populations. Genetics 75:213–219

    PubMed  CAS  Google Scholar 

  • Nordborg M, Tavaré S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190–193

    Article  PubMed  CAS  Google Scholar 

  • Nsengimana J, Baret P, Haley CS, Visscher PM (2004) Linkage disequilibrium in the domesticated pig. Genetics 166:1395–1404

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Przeworski M (2001) Linkage disequilibrium in humans: models and data. Am J Hum Genet 69:1–14

    Article  PubMed  CAS  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler IV ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Nat Acad Sci USA 98:11479–11484

    Article  PubMed  CAS  Google Scholar 

  • Riaz S, Dangl GS, Edwards KJ, Meredith CP (2004) A microsatellite based framework linkage map of Vitis vinifera L.. Theor Appl Genet 108:864–872

    Article  PubMed  CAS  Google Scholar 

  • Schoen D, Brown A (1993) Conservation of allelic richness in wild crop relatives is aided by assessment of genetic markers. Proc Nat Acad Sci USA 22:10623–10627

    Article  Google Scholar 

  • Sefc KM, Lopes MS, Lefort F, Botta R, Roubelakis-Angelakis KA, Ibanez J, Pejic I, Wagner HW, Glossl J, Steinkellner H (2000) Microsatellite variability in grapevine cultivars from different European regions and evaluation of assignment testing to assess the geographic origin of cultivars. Theor Appl Genet 100:498–505

    Article  Google Scholar 

  • Simko I (2004) One potato, two potato: haplotype association mapping in autotetraploids. Trends Plant Sci 9:441–448

    Article  PubMed  CAS  Google Scholar 

  • StatSoft France (2005). STATISTICA (logiciel d’analyse de données), version 7.1. http://www.statsoft.fr

  • Stich B, Melchinger AE, Frisch M, Maurer HP, Heckenberger M, Reif JC (2005) Linkage disequilibrium in European elite maize germplasm investigated with SSRs. Theor Appl Genet 111:723–730

    Article  PubMed  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  PubMed  CAS  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction. Am J Hum Genet 73:1162–1169

    Article  PubMed  CAS  Google Scholar 

  • Stumpf MPH, Goldstein DB (2003) Demography, recombination hotspot intensity, and the block structure of linkage disequilibrium. Curr Biol 13:1–8

    Article  PubMed  CAS  Google Scholar 

  • Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Nat Acad Sci USA 98:9161–9166

    Article  PubMed  CAS  Google Scholar 

  • Tenesa A, Knott SA, Ward D, Smith D, Williams JL, Visscher PM (2003) Estimation of linkage disequilibrium in a sample of the United Kingdom dairy cattle population using unphased genotypes. J Anim Sci 81:617–623

    PubMed  CAS  Google Scholar 

  • Weir SB, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Weir SB (1996) Genetic data analysis II. Sinauer Associates, Inc., Sunderland, pp 91–138

    Google Scholar 

  • Zapata C (2000) The D’ measure of overall gametic disequilibrium between pairs of multiallelic loci. Evolution 54:1809–1812

    PubMed  CAS  Google Scholar 

  • Zhu YL, Song QJ, Hyten DL, Van Tassell CP, Matukumalli LK, Grimm DR, Hyatt SM, Fickus EW, Young ND, Cregan PB (2003) Single-nucleotide polymorphisms in soybean. Genetics 163:1123–1134

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by INRA. We thank D. Vares for Vassal collection plant and data management, V. Laucou for providing the DNA, T. Bataillon for his help with Mstrat, and two anonymous reviewers, B. Courtois, M. Deu, V. Laucou, J. P. Péros, and H. A. Tsitrone for useful comments on a previous version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Agnès Doligez.

Additional information

Communicated by A. Charcosset

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barnaud, A., Lacombe, T. & Doligez, A. Linkage disequilibrium in cultivated grapevine, Vitis vinifera L. Theor Appl Genet 112, 708–716 (2006). https://doi.org/10.1007/s00122-005-0174-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-005-0174-1

Keywords

Navigation