Theoretical and Applied Genetics

, Volume 115, Issue 6, pp 837–847

Linkage disequilibrium in synthetic varieties of perennial ryegrass

Original Paper

Abstract

Synthetic varieties obtained after three to four panmictic generations are variable, not structured and so can be used for association studies. The pattern of linkage disequilibrium (LD) decay determines whether a genome scan or a candidate gene approach can be used for an association study between genotype and phenotype. Our goal was to evaluate the effect of the number of parents used to build the synthetic varieties on the pattern of LD decay. LD was investigated in the gibberelic acid insensitive gene (GAI) region in three synthetic varieties of perennial ryegrass (Lolium perenne L.) chosen for their contrasted number of parents in the initial polycrosses. Results were compared with those obtained from a core collection. STS and SSR markers were used to evaluate variation, structuration and LD in each variety. As expected, the varieties variability increased with the number of parents almost up to the core collection variability. No structuration was observed in the varieties. Significant LDs were observed up to 1.6 Mb in a variety originated from six related parents and not above 174 kb in a variety originated from 336 parents. These results suggest that a candidate gene approach can be used when varieties have a large number of parents and a genome scan approach can be envisaged in specific regions when varieties have a low number of parents. Nevertheless, we strongly recommend to estimate the pattern of LD decay in the population and in the genomic region studied before performing an association study.

References

  1. Alm V, Fang C, Busso CS, Devos KM, Vollan K, Grieg Z, Rognli OA (2003) A linkage map of meadow fescue (Festuca pratensis Huds.) and comparative mapping with other Poaceae species. Theor Appl Genet 108:25–40PubMedCrossRefGoogle Scholar
  2. Ardlie KG, Kruglyak L, Seielstad M (2002) Patterns of linkage disequilibrium in the human genome. Nat Rev Genet 3:299–309PubMedCrossRefGoogle Scholar
  3. Balfourier F, Charmet G, Ravel C (1998) Genetic differentiation within and between natural populations of perennial and annual ryegrass (Lolium perenne and L. rigidum). Heredity 81:100–110CrossRefGoogle Scholar
  4. Barre P, Darrieutort G, Auzanneau J, Julier B (2005) Development and use of a tool for automated alignments of genes in the rice BAC’s GenBank card against other species. Fourth symposium of Molecular Breeding of Forage and Turf, a satellite workshop of the XXth International Grassland Congress, Aberystwyth, WalesGoogle Scholar
  5. Barre P, Emile JC, Betin M, Surault F, Ghesquière M, Hazard L (2006) Morphological characteristics of perennial ryegrass leaves that influence short-term intake in dairy cows. Agron J 98:978–985CrossRefGoogle Scholar
  6. Belkhir K, Borsa P, Chikhi L (2004) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier, FranceGoogle Scholar
  7. Bennett MD, Leitch IJ (2005) Nuclear DNA amounts in angiosperms: progress, problems and prospects. Ann Bot 95:45–90PubMedCrossRefGoogle Scholar
  8. Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31:24–28PubMedGoogle Scholar
  9. Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Charcosset A (2004) Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168:2169–2185PubMedCrossRefGoogle Scholar
  10. Cheung WY, Hubert N, Landry BS (1993) A simple and rapid DNA microextraction method for plant, animal and insect suitable for RAPD and other PCR analyses. PCR Methods Appl 3:69–70PubMedGoogle Scholar
  11. Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374PubMedCrossRefGoogle Scholar
  12. Gallais A (2003) Quantitative genetics and breeding methods in autopolyploid plants. INRA, Paris, pp 66–68Google Scholar
  13. Gaut BS, Long AD (2003) The lowdown on linkage disequilibrium. Plant Cell 15:1502–1506PubMedCrossRefGoogle Scholar
  14. Ghariani S, Trifi-Farah N, Chakroun M, Marghali S, Marrakchi M (2003) Genetic diversity in Tunisian perennial ryegrass revealed by ISSR markers. Gen Resour Crop Evol 50:809–815CrossRefGoogle Scholar
  15. Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485PubMedCrossRefGoogle Scholar
  16. Guthridge K, Dupal M, Kolliker R, Jones E, Smith K, Forster J (2001) AFLP analysis of genetic diversity within and between populations of perennial ryegrass (Lolium perenne L.). Euphytica 122:191–201CrossRefGoogle Scholar
  17. Harmegnies N, Farnir F, Davin F, Buys N, Georges M, Coppieters W (2006) Measuring the extent of linkage disequilibrium in commercial pig populations. Anim Genet 37:225–231PubMedCrossRefGoogle Scholar
  18. Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. TAG Theor Appl Genet 38:226–231CrossRefGoogle Scholar
  19. Jensen LB, Andersen J, Frei U, Xing Y, Taylor C, Holm P, Lubberstedt T (2005a) QTL mapping of vernalization response in perennial ryegrass (Lolium perenne L.) reveals co-location with an orthologue of wheat VRN1. Theor Appl Genet 110:527–536PubMedCrossRefGoogle Scholar
  20. Jensen LB, Muylle H, Arens P, Andersen CH, Holm PB, Ghesquière M, Julier B, Lubberstedt T, Nielsen KK, De Riek J, Roldan-Ruiz I, Roulund N, Taylor C, Vosman B, Barre P (2005b) Development and mapping of a public reference set of SSR markers in Lolium perenne L. Mol Ecol Notes 5:951–957CrossRefGoogle Scholar
  21. 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 109:681–689PubMedCrossRefGoogle Scholar
  22. Kubik C, Sawkins M, Meyer WA, Gaut BS (2001) Genetic diversity in seven perennial ryegrass (Lolium perenne L.) cultivars based on SSR markers. Crop Sci 41:1565–1572CrossRefGoogle Scholar
  23. Lauvergeat V, Barre P, Bonnet M, Ghesquière M (2005) Sixty simple sequence repeats (SSR) markers for use in the Festuca/Lolium complex of grasses. Mol Ecol Notes 5:401–405CrossRefGoogle Scholar
  24. Liu A, Burke JM (2006) Patterns of nucleotide diversity in wild and cultivated sunflower. Genetics 173:321–330PubMedCrossRefGoogle Scholar
  25. Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12(2):57–63. doi:10.1016/j.tplants.2006.12.001 Google Scholar
  26. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  27. Ogawa M, Kusano T, Katsumi M, Sano H (2000) Rice gibberellin-insensitive gene homolog, OsGAI encodes a nuclear-localized protein capable of gene activation at transcriptional level. Gene 245:21–29PubMedCrossRefGoogle Scholar
  28. Peng JR, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205PubMedGoogle Scholar
  29. Peng JR, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261PubMedCrossRefGoogle Scholar
  30. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909PubMedCrossRefGoogle Scholar
  31. Pritchard JK, Stephens M, Donnelly P (2000a) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  32. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000b) Association mapping in structured populations. Am J Human Genet 67:170–181CrossRefGoogle Scholar
  33. Rafalski A (2002) Application of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 54:94–100CrossRefGoogle Scholar
  34. Raymond M, Rousset F (1995) GENEPOP (Version1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  35. Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484PubMedCrossRefGoogle Scholar
  36. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  37. Saghai-Maroof MA, Soliman K, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. PNAS 81:8014–8018PubMedCrossRefGoogle Scholar
  38. Skot L, Humphreys MO, Armstead I, Heywood S, Skot KP, Sanderson R, Thomas ID, Chorlton KH, Sackville Hamilton NR (2005) An association mapping approach to identify flowering time genes in natural populations of Lolium perenne (L.) Mol Breed 15:233–245CrossRefGoogle Scholar
  39. Tenaillon MI, Sawkins MC, Anderson LK, Stack SM, Doebley J, Gaut BS (2002) Patterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp mays L.). Genetics 162:1401–1413PubMedGoogle Scholar
  40. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  41. Weising K, Beyermann B, Ramser J, Kahl G (1991) Plant DNA fingerprinting with radioactive and digoxignated oligonucleotide probes complementary to simple repetitive DNA sequences. Electrophoresis 12:159–169PubMedCrossRefGoogle Scholar
  42. Yamada T, Forster JW (2005) QTL analysis and trait dissection in ryegrass (Lolium spp.). Fourth symposium of Molecular Breeding of Forrage and Turf, a satellite workshop of the XXth International Grassland Congress, Aberystwyth, WalesGoogle Scholar
  43. Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.INRA, Unité de Génétique et d’Amélioration des Plantes FourragèresLusignanFrance

Personalised recommendations