Skip to main content

Advertisement

Log in

SNP discovery, validation, haplotype structure and linkage disequilibrium in full-length herbage nutritive quality genes of perennial ryegrass (Lolium perenne L.)

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Development of accurate high-throughput molecular marker systems such as SNPs permits evaluation and selection of favourable gene variants to accelerate elite varietal production. SNP discovery in perennial ryegrass has been based on PCR amplification and sequencing of multiple amplicons designed to scan all components of the transcriptional unit. Full-length genes (with complete intron–exon structure and promoter information) corresponding to well-defined biochemical functions such as lignin biosynthesis and oligosaccharide metabolism are ideal for complete SNP haplotype determination. Multiple SNPs at regular intervals across the transcriptional unit were detected within and between the heterozygous parents and validated in the progeny of the F 1(NA6 × AU6) genetic mapping family. Haplotype structures in the parental genotypes were defined and haplotypic abundance, structure and variation were assessed in diverse germplasm sources. Decay of LD to r 2 values of c. 0.2 typically occurs over 500–3,000 bp, comparable with gene length and with little apparent variation between diverse, ecotypic and varietal population sub-groups. Similar patterns were revealed as limited blocks of intragenic LD. The results are compatible with the reproductive biology of perennial ryegrass and the effects of large ancestral population size. This analysis provides crucial information to validate strategies for correlation of haplotypic diversity and phenotypic variation through association mapping.

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

Access this article

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andersen JR, Lübberstedt T (2003) Functional markers in plants. Trends Plant Sci 8:554–560

    Article  PubMed  CAS  Google Scholar 

  • Armstead IP, Turner LB, Farrell M, Skøt L, Gomez P, Montoya T, Donnison IS, King IP, Humphreys MO (2004) Synteny between a major heading-date QTL in perennial ryegrass (Lolium perenne L.) and the Hd3 heading-date locus in rice. Theor Appl Genet 108:822–828

    Article  PubMed  CAS  Google Scholar 

  • Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualisation of LD and haplotype maps. Bioinformatics 21:263–265

    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 Natl Acad Sci USA 101:15255–15260

    Article  PubMed  CAS  Google Scholar 

  • Buxton DR, Russell JR (1988) Lignin constituents and cell-wall digestibility of grass and legume stems. Crop Sci 28:553–558

    Article  CAS  Google Scholar 

  • Chalmers J, Johnson X, Lidgett A, Spangenberg GC (2003) Isolation and characterisation of a sucrose:sucrose 1-fructosyltransferase gene from perennial ryegrass (Lolium perenne L.). J Plant Physiol 160:1385–1391

    Article  PubMed  CAS  Google Scholar 

  • Chalmers J, Lidgett A, Johnson X, Jennings K, Cummings N, Forster J, Spangenberg G (2005) Molecular genetics of fructan metabolism in temperate grasses. Plant Biotech J 3:459–474

    Article  CAS  Google Scholar 

  • Cogan NOI, Smith KF, Yamada T, Francki MG, Vecchies AC, Jones ES, Spangenberg GC, Forster JW (2005) QTL analysis and comparative genomics of herbage quality traits in perennial ryegrass (Lolium perenne L.). Theor Appl Genet 110:364–380

    Article  PubMed  CAS  Google Scholar 

  • Cogan NOI, Ponting RC, Vecchies AC, Drayton MC, George J, Dobrowolski MP, Sawbridge TI, Spangenberg GC, Smith KF, Forster JW (2006) Gene-associated single nucleotide polymorphism (SNP) discovery in perennial ryegrass (Lolium perenne L.). Mol Genet Genom 276:101–112

    Article  CAS  Google Scholar 

  • Cornish MA, Hayward MD, Lawrence MJ (1979) Self-incompatibility in ryegrass. I. Genetic control in diploid Lolium perenne L. Heredity 43:95–106

    Google Scholar 

  • Devey F, Fearon CH, Hayward MD, Lawrence MJ (1994) Self-incompatibility in ryegrass. 11. Number and frequency of alleles in a cultivar of Lolium perenne L. Heredity 73:262–264

    Google Scholar 

  • Dobrowolski MP, Forster JW (2007) Chapter 9: Linkage disequilibrium-based association mapping in forage species. In: Oraguzie NC, Rikkerink E, Gardiner SE, De Silva NH (eds) Association mapping in plants. Springer, New York, pp 197–209

    Chapter  Google Scholar 

  • Faville M, Vecchies AC, Schreiber M, Drayton MC, Hughes LJ, Jones ES, Guthridge KM, Smith KF, Sawbridge T, Spangenberg GC, Bryan GT, Forster JW (2004) Functionally-associated molecular genetic marker map construction in perennial ryegrass (Lolium perenne L.). Theor Appl Genet 110:12–32

    Article  PubMed  CAS  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ESI (2003) Structure of linkage disequilibrium in plants. Ann Rev Plant Biol 54:357–374

    Article  CAS  Google Scholar 

  • Forster JW, Jones ES, Batley J, Smith KF (2004) Molecular marker-based genetic analysis of pasture and turf grasses. In: Hopkins A, Wang Z-Y, Sledge M, Barker RE (eds) Molecular breeding of forage and turf. Kluwer, Dordrecht, pp 197–239

    Chapter  Google Scholar 

  • Fredman D, White SJ, Potter S, Eichler EE, Den Dunnen JT, Brookes AJ (2004) Complex SNP-related sequence variation in segmental genome duplications. Nat Genet 36:861–866

    Article  PubMed  CAS  Google Scholar 

  • Gallagher JA, Pollock CJ (1998) Isolation and characterisation of a cDNA clone from Lolium temulentum L. encoding for a sucrose hydrolytic enzyme which shows alkaline/neutral invertase activity. J Exp Bot 49:789–795

    Article  CAS  Google Scholar 

  • Gallagher JA, Cairns AJ, Pollock CJ (2004) Cloning and characterisation of a putative fructosyltransferase and two putative invertase genes from the temperate grass Lolium temulentum L. J Exp Bot 55:557–569

    Article  PubMed  CAS  Google Scholar 

  • Guthridge KM, Dupal MD, Kölliker R, Jones ES, Smith KF, Forster JW (2001) AFLP analysis of genetic diversity within and between populations of perennial ryegrass (Lolium perenne L.). Euphytica 122:191–201

    Article  CAS  Google Scholar 

  • Hayes BJ, Visscher PM, McPartlan HC, Goddard ME (2003) Novel multilocus measure of linkage disequilibrium to estimate past effective population size. Genome Res 13:635–643

    Article  PubMed  CAS  Google Scholar 

  • Heath R, Huxley H, Stone B, Spangenberg G (1998) cDNA cloning and differential expression of three caffeic acid O-methyltransferase homologues from perennial ryegrass (Lolium perenne L.). J Plant Physiol 153:649–657

    CAS  Google Scholar 

  • Heath R, McInnes R, Lidgett A, Huxley H, Lynch D, Jones ES, Mahoney NL, Spangenberg GC (2002) Isolation and characterisation of three 4-coumarate:CoA-ligase homologue cDNAs from perennial ryegrass (Lolium perenne L.). J Plant Physiol 159:773–779

    Article  CAS  Google Scholar 

  • Heuertz M, De Paoli E, Kallman T, Larsson H, Jurman I, Morgante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce (Picea abies [L.] Karst). Genetics 174:2095–2105

    Article  PubMed  CAS  Google Scholar 

  • Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Pop Biol 33:54–78

    Article  CAS  Google Scholar 

  • Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953

    Article  PubMed  CAS  Google Scholar 

  • Johnson X, Lidgett A, Chalmers J, Guthridge K, Jones E, Spangenberg GC (2003) Isolation and characterisation of an invertase gene from perennial ryegrass (Lolium perenne L.). J Plant Physiol 160:903–911

    Article  PubMed  CAS  Google Scholar 

  • Jones RN, Rees H (1966) Chiasma frequencies and the potential genetic variability of Lolium populations. Nature 211:432–433

    Article  Google Scholar 

  • Jones EL, Roberts E (1991) A note on the relationship between palatability and water-soluble carbohydrates in perennial ryegrass. Irish J Agric Res 30:163–167

    CAS  Google Scholar 

  • Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold hardiness and wood quality-related candidate genes in Douglas fir. Genetics 171:2368–2378

    Article  CAS  Google Scholar 

  • Lidgett A, Jennings K, Johnson X, Guthridge K, Jones E, Spangenberg G (2002) Isolation and characterisation of fructosyltransferase gene from perennial ryegrass (Lolium perenne). J Plant Physiol 159:415–422

    Article  Google Scholar 

  • Lynch D, Lidgett A, McInnes R, Huxley H, Jones E, Mahoney N, Spangenberg G (2002) Isolation and characterisation of three cinnamyl alcohol dehydrogenase homologue cDNAs from perennial ryegrass (Lolium perenne L.). J Plant Physiol 159:653–660

    Article  CAS  Google Scholar 

  • Mackay TFC (2001) The genetic architecture of quantitative traits. Ann Rev Genet 35:303–309

    Article  PubMed  CAS  Google Scholar 

  • McInnes R, Lidgett A, Lynch D, Huxley H, Jones E, Mahoney N, Spangenberg G (2002) Isolation and characterisation of a cinnamoyl-CoA reductase gene from perennial ryegrass (Lolium perenne). J Plant Physiol 159:415–422

    Article  CAS  Google Scholar 

  • Michell PJ (1973) Relations between fibre and water soluble carbohydrate contents of pasture species and their digestibility and voluntary intake by sheep. Aust J Exp Agric Anim Husb 13:165–170

    Article  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330

    Article  PubMed  CAS  Google Scholar 

  • Olsen KM, Halldorsdottir SS, Stinchcombe JR, Weinig C, Schmitt J, Purugganan MD (2004) Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles. Genetics 167:1361–1367

    Article  PubMed  CAS  Google Scholar 

  • Rees H, Ahmad K (1963) Chiasma frequencies in Lolium populations. Evolution 17:575–579

    Article  Google Scholar 

  • Rees H, Dale PJ (1974) Chiasmata and variability in Lolium and Festuca populations. Chromosoma 47:335–351

    Article  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 Natl Acad Sci USA 98:11479–11484

    Article  PubMed  CAS  Google Scholar 

  • Sackville-Hamilton NR, Skøt L, Chorlton KH, Thomas ID, Mizen S (2002) Molecular genecology of temperature response in Lolium perenne:1. Preliminary analysis to reduce false positives. Mol Ecol 11:1855–1863

    Article  PubMed  CAS  Google Scholar 

  • Simko I, Haynes KG, Jones RW (2006) Assessment of linkage disequilibrium in potato genome with single nucleotide polymorphism markers. Genetics 173:2237–2245

    Article  PubMed  CAS  Google Scholar 

  • Skøt L, Sackville-Hamilton NR, Mizen S, Chorlton KH, Thomas ID (2002) Molecular genecology of temperature response in Lolium perenne: 2. Association of AFLP markers with ecogeography. Mol Ecol 11:1865–1876

    Article  PubMed  Google Scholar 

  • Skøt L, Humphreys J, Armstead IP, Humphreys MO, Gallagher JA, Thomas ID (2005a) Approaches for associating molecular polymorphisms with phenotypic traits based on linkage disequilibrium in natural populations of Lolium perenne. In: Humphreys MO (eds) Molecular breeding of the genetic improvement of forage crops and turf. Wageningen Academic Publishers, Netherlands, pp 157

    Google Scholar 

  • Skøt L, Humphreys MO, Armstead I, Heywood S, Skøt KP, Sanderson R, Thomas ID, Chorlton KH, Sackville-Hamilton NR (2005b) An association mapping approach to identify flowering time genes in natural populations of Lolium perenne (L.). Mol Breed 15:233–245

    Article  CAS  Google Scholar 

  • Smith KF, Reed KFM, Foot JZ (1997) An assessment of the relative importance of specific traits for the genetic improvement of nutritive value in dairy pasture. Grass Forage Sci 52:167–75

    Article  Google Scholar 

  • Sorrells ME, Wilson WA (1997) Direct classification and selection of superior alleles for crop improvement. Crop Sci 37:691–697

    Article  Google Scholar 

  • Spangenberg GC, Forster JW, Edwards D, John U, Mouradov A, Emmerling M, Batley J, Felitti S, Cogan NOI, Smith KF, Dobrowolski MP (2005). Future directions in the molecular breeding of forage and turf. In: Humphreys MO (eds) Molecular breeding of the genetic improvement of forage crops and turf. Wageningen Academic Publishers, Netherlands, pp 83–97

    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 

  • Yamada T, Forster JW, Humphreys MW, Takamizo T (2005) Genetics and molecular breeding in the Lolium/Festuca pasture grass species complex. Grassland Sci 51:89–106

    Article  CAS  Google Scholar 

  • Zein I, Wenzel G, Andersen JR, Lübberstedt T (2007) Low level of linkage disequilibrium at the COMT (caffeic acid O-methyltransferase) locus in European maize (Zea mays L.). Genetic Res Crop Evol 54:139–148

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by funding from the Victorian Department of Primary Industries, Dairy Australia Ltd., the Geoffrey Gardiner Dairy Foundation, Meat and Livestock Australia Ltd. and the Molecular Plant Breeding Cooperative Research Centre. The authors thank Prof. Michael Hayward and Dr. Ben Hayes for careful critical assessment of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John W. Forster.

Additional information

Communicated by R. Waugh.

Electronic supplementary material

Below is the link to the electronic supplementary material.

438_2007_275_MOESM1_ESM.doc

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ponting, R.C., Drayton, M.C., Cogan, N.O.I. et al. SNP discovery, validation, haplotype structure and linkage disequilibrium in full-length herbage nutritive quality genes of perennial ryegrass (Lolium perenne L.). Mol Genet Genomics 278, 585–597 (2007). https://doi.org/10.1007/s00438-007-0275-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-007-0275-4

Keywords

Navigation