Abstract
A molecular marker-based map of perennial ryegrass (Lolium perenne L.) has been constructed through the use of polymorphisms associated with expressed sequence tags (ESTs). A pair-cross between genotypes from a North African ecotype and the cultivar Aurora was used to generate a two-way pseudo-testcross population. A selection of 157 cDNAs assigned to eight different functional categories associated with agronomically important biological processes was used to detect polymorphic EST•RFLP loci in the F1(NA6 í AU6) population. A comprehensive set of EST•SSR markers was developed from the analysis of 14,767 unigenes, with 310 primer pairs showing efficient amplification and detecting 113 polymorphic loci. Two parental genetic maps were produced: the NA6 genetic map contains 88 EST•RFLP and 71 EST•SSR loci with a total map length of 963 cM, while the AU6 genetic map contains 67 EST•RFLP and 58 EST•SSR loci with a total map length of 757 cM. Bridging loci permitted the alignment of homologous chromosomes between the parental maps, and a sub-set of genomic DNA-derived SSRs was used to relate linkage groups to the perennial ryegrass reference map. Regions of segregation distortion were identified, in some instances in common with other perennial ryegrass maps. The EST-derived marker-based map provides the basis for in silico comparative genetic mapping, as well as the evaluation of co-location between QTLs and functionally associated genetic loci.
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Altschul SF, Madden Tl, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389•3402
Areshchenkova T, Ganal M (2002) Comparative analysis of polymorphism and chromosomal location of tomato microsatellite markers isolated from different sources. Theor Appl Genet 104:229•235
Armstead IP, Turner LB, King IP, Cairns AJ, Humphreys MO (2002) Comparison and integration of genetic maps generated from F2 and BC1-type mapping populations in perennial ryegrass. Plant Breed 121:501•507
Arnold C, Rossetto M, McNally J, Henry RJ (2002) The application of SSRs characterized for grape (Vitis vinifera) to conservation studies in Vitaceae. Am J Bot 89:22•28
Barrett B, Griffiths A, Schreiber M, Ellison N, Mercer C, Bouton J, Ong B, Forster J, Sawbridge T, Spangenberg G, Bryan G, Woodfield D (2004) A microsatellite map of white clover. Theor Appl Genet 109:596•608
Barth S, Melchinger AE, Devezi-Savula B, Lubberstedt T (2001) Influence of genetic background and heterozygosity on meiotic recombination in Arabidopsis thaliana. Genome 44:971•978
Bert PF, Charmet G, Sourdille P, Hayward MD, Balfourier F (1999) A high-density molecular map for ryegrass (Lolium perenne) using AFLP markers. Theor Appl Genet 99:445•452
Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004•1010
Buxton DR, Russell JR (1988) Lignin constituents and cell-wall digestibility of grass and legume stems. Crop Sci 28:553•558
Chao S, Baysdorfer C, Heredia-Diaz O, Musket T, Xu G, Coe EH Jr (1994) RFLP mapping of partially sequenced leaf cDNA clones in maize. Theor Appl Genet 88:717•721
Chen M, Presting G, Barbazuk WB, Goicoechea JL, Blackmon B, Fang G, Kim H, Frisch D, Yu Y, Sun S (2002) An integrated physical and genetic map of the rice genome. Plant Cell 14:521•523
Chen X, Salamini F, Gebhardt C (2001) A potato molecular-function map for carbohydrate metabolism and transport. Theor Appl Genet 102:284•295
Cho YG, Ishii T, Temnykh S, Chen X, Lipovich L, McCouch SR, Park WD, Ayres N, Cartinhour S (2000) Diversity of microsatellites derived from genomic libraries and GenBank sequences in rice (Oryza sativa L.). Theor Appl Genet 100:713•722
Cordeiro GM, Casu R, McIntyre CL, Manners JM, Henry RJ (2001) Microsatellite markers from sugarcane (Saccharum spp.) ESTs cross transferable to Erianthus and sorghum. Plant Sci 160:1115•1123
Decroocq V, Favèc) M, Hagen L, Bordenhave L, Decroocq S (2003) Development and transferability of apricot and grape EST microsatellite markers across taxa. Theor Appl Genet 106:912•922
Dumsday JL, Smith KF, Forster JW, Jones ES (2003) SSR-based genetic linkage analysis of resistance to crown rust (Puccinia coronata f.sp. lolii) in perennial ryegrass (Lolium perenne L.). Plant Pathol 52:628•637
Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295•307
Eujayl I, Sorrells ME, Baum M, Wolters P, Powell W (2002) Assessment of genotypic variation among cultivated durum wheat based on EST•SSRs. Euphytica 119:39•43
Feinberg AP, Vogelstein B (1984) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6•13
Forster JW, Jones ES, Kölliker R, Drayton MC, Dupal MP, Guthridge KM, Smith KF (2001) DNA profiling in outbreeding forage species. In: Henry R (ed) Plant genotyping•the DNA fingerprinting of plants. CABI, Wallingford, pp 299•320
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
Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207•209
Giddings G (2000) Modelling the spread of pollen from Lolium perenne. The implications for the release of wind-pollinated transgenics. Theor Appl Genet 100:971•974
Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121•1137
Griffiths AG, Barrett BA, Ellison N, Sawbridge T, Spangenberg G, Bryan GJ, Schreiber M (2002) Getting out there: transportability of white clover EST and genomic DNA-derived microsatellites. In: Proceedings of the 12th Australasian plant breeding conference, Perth, 15•20 September 2002, pp 69•72
Hackauf B, Wehling P (2002) Identification of microsatellite polymorphisms in an expressed portion of the rye genome. Plant Breed 121:17•25
Hackett CA, Broadfoot LB (2003) Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps. Heredity 90:33•38
Hadad RG, Pfeiffer TW, Poneleit CG (1996) Repeatability and heritability of divergent recombination frequencies in the Iowa Stiff Stalk Synthetic (Zea mays L.). Theor Appl Genet 93:990•996
Haldane JBS (1919) The combination of linkage values and the calculation of distances between the loci of linked factors. J Genet 8:299•309
Hayward MD, Forster JW, Jones JG, Dolstra O, Evans C, McAdam NJ, Hossain KG, Stammers M, Will J, Humphreys MO, Evans GM (1998) Genetic analysis of Lolium. I. Identification of linkage groups and the establishment of a genetic map. Plant Breed 117:451•455
Holton TA, Christopher JT, McClure L, Harker N, Henry RJ (2002) Identification and mapping of polymorphic SSR markers from expressed gene sequences of barley and wheat. Mol Breed 9:63•71
Jenczewski E, Gherardi M, Bonnin I, Prosperi JM, Olivieri I, Huguet T (1997) Insight on segregation distortions in two intraspecific crosses between annual species of Medicago (Leguminosae). Theor Appl Genet 94:682•691
Johnson X, Lidgett A, Chalmers J, Guthridge K, Jones E, Cummings N, Spangenberg G (2003) Isolation and characterisation of an invertase cDNA from perennial ryegrass (Lolium perenne L.). J Plant Physiol 160:903•911
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
Jones ES, Dupal MP, Kölliker R, Drayton MC, Forster JW (2001) Development and characterisation of simple sequence repeat (SSR) markers for perennial ryegrass (Lolium perenne L.). Theor Appl Genet 102:405•415
Jones ES, Mahoney NL, Hayward MD, Armstead IP, Jones JG, Humphreys MO, King IP, Kishida T, Yamada T, Balfourier F, Charmet C, Forster JW (2002a) An enhanced molecular marker-based map of perennial ryegrass (Lolium perenne L.) reveals comparative relationships with other Poaceae species. Genome 45:282•295
Jones ES, Dupal MD, Dumsday JL, Hughes LJ, Forster JW (2002b) An SSR-based genetic linkage map for perennial ryegrass (Lolium perenne L.). Theor Appl Genet 105:577•584
Kantety RV, La Rota M, Matthews DE, Sorrells ME (2002) Data mining for simple sequence repeats in expressed sequence tags from barley, maize, rice, sorghum and wheat. Plant Mol Biol 48:501•510
Knox MR, Ellis THN (2002) Excess heterozygosity contributes to genetic map expansion in pea recombinant inbred populations. Genetics 162:861•873
Kurata N, Nagamura Y, Yamamoto K, Harushima Y, Sue N, Wu J, Antonio BA, Shomura A, Shimizu T, Lin S-Y, Inoue T, Fukuda A, Shimano T, Kuboki Y, Toyama T, Miyamoto Y, Kirihara T, Hayasaka K, Miyao A, Monna L, Zhong HS, Tamura Y, Wang Z-X, Momma T, Umehara Y, Yano M, Sasaki T, Minobe Y (1994) A 300-kilobase-interval genetic map of rice including 883 expressed sequences. Nat Genet 8:365•372
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary linkage maps of experimental and natural populations. Genomics 1:174•181
Li X, Song Y, Century K, Straight S, Ronald P, Dong X, Lassner M, Zhang Y (2001) A fast neutron deletion mutagenesis-based reverse genetics systems for plants. Plant J 27:235•242
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 159:1037•1043
Maliepaard C, van Ooijen JW (1994) QTL mapping in a full-sib family of an outcrossing species. In: van Ooijen JW, Jansen J (eds) Biometrics in plant breeding: applications of molecular markers. In: Proceedings of the 9th meeting of Eucarpia section biometrics, pp 140•146
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
Metzgar D, Bytof J, Wills C (2000) Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Res 10:72•80
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
Mogg R, Batley J, Hanley S, Edwards D, O tm)Sullivan H, Edwards KJ (2002) Characterisation of the flanking regions of Zea mays microsatellites reveals a large number of useful sequence polymorphisms. Theor Appl Genet 105:532•543
Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30:194•200
Plummer RM, Hall RL, Watt TA (1990) The influence of crown rust (Puccinia coronata var lolii) on tiller production and survival of perennial ryegrass (Lolium perenne L.) plants in simulated swards. Grass Forage Sci 45:9•16
Potter LR (1987) Effect of crown rust on regrowth, competitive ability and nutritional quality of perennial and Italian ryegrass. Plant Pathol 36:455•461
Potter LR, Cagas B, Paul VH, Birckenstaedt E (1990) Pathogenicity of some European collections (Puccinia coronata Corda) on cultivars of perennial ryegrass. J Phytopathol 130:119•126
Price T (1987) Ryegrass rust in Victoria. Plant Prot Q 2:189
Prioul JL, Pelleschi S, Sèc)ne M, Thèc)venot C, Causse M, de Vienne D, Leonard A (1999) From QTLs for enzyme activity to candidate genes in maize. J Exp Bot 50:1281•1288
Qi L, Echalier B, Friebe B, Gill BS (2003) Molecular characterisation of a set of wheat deletion stocks for use in chromosome bin mapping of ESTs. Funct Integr Genomics 3:39•55
Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94•1000
Rees H, Thompson JB (1956) Genotypic control of chromosome behaviour in rye. III. Chiasma frequency on homozygotes and heterozygotes. Heredity 10:409•424
Säll T (1990) Genetic control of recombination in barley. II. Variation in linkage between marker genes. Hereditas 112:171•178
Sawbridge T, Ong E-K, Binnion C, Emmerling M, McInnes R, Meath K, Nguyen N, Nunan K, O tm)Neill M, O tm)Toole F, Rhodes C, Simmonds J, Tian P, Wearne K, Webster T, Winkworth A, Spangenberg G (2003) Generation and analysis of expressed sequence tags in perennial ryegrass (Lolium perenne L.). Plant Sci 165:1089•1100
Schneider K, Borchardt DC, Schäfer-Pregl R, Nagl N, Glass C, Jeppsson A, Gebhardt C, Salamini F (1999) PCR-based cloning and segregation analysis of functional gene homologues in Beta vulgaris. Mol Gen Genet 262:515•524
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233•234
Scott KD, Eggler P, Seaton G, Rossetto M, Ablett EM, Lee LS, Henry RJ (2000) Analysis of SSRs derived from grape ESTs. Theor Appl Genet 100:723•726
Sebastian RL, Howell EC, King GJ, Marshall DF, Kearsey MJ (2000) An integrated AFLP and RFLP Brassica oleracea linkage map from two morphologically distinct doubled-haploid mapping populations. Theor Appl Genet 100:75•81
Sharopova N, McMullen MD, Schultz L, Schroeder S, Sanchez-Villeda H, Gardiner J, Bergstrom D, Houchins K, Melia-Hancock S, Musket T, Duru N, Polacco M, Edwards K, Ruff T, Register JC, Brouwer C, Thompson R, Velasco R, Chin E, Lee M, Woodman-Clikeman W, Long MJ, Liscum E, Cone K, Davis G, Coe EH Jr (2002) Development and mapping of SSR markers for maize. Plant Mol Biol 48:463•481
Sharp PJ, Kreis M, Shewry PR, Gale MD (1988) Location of β-amylase sequences in wheat and its relatives. Theor Appl Genet 75:286•290
Sorrells ME, Wilson WA (1997) Direct classification and selection of superior alleles for crop improvement. Crop Sci 37:691•697
Sorrells ME, La Rota M, Bermundez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Miftahudin, Mahmoud A, Ma X, Gustafson PJ, Qi LL, Echalier B, Gill BS, Matthews DE, Lazo GR, Chao S, Anderson OD, Edwards H, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvorak J, Zhang D, Nguyen HT, Peng J, Lapitan NLV, Gonzalez-Hernandez JL, Anderson JA, Hossain K, Kalavacharla V, Kianian SF, Choi D-W, Close TJ, Bilbirgi M, Gill KS, Steber C, Walker-Simmons MK, McGuire PE, Qualset CO (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818•1827
Squirrel J, Hollingsworth PM, Woodhead M, Russell J, Lowe AJ, Gibby M, Powell W (2003) How much effort is required to isolate nuclear microsatellites from plants? Mol Ecol 12:1339•1348
Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Röder MS, Wing RA, Wu W, Young ND (1992) High-density molecular genetic linkage maps of the tomato and potato genomes. Genetics 132:1141•1160
Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441•1452
Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterisation of gene-derived SSR markers in barley (Hordeum vulgare L.) Theor Appl Genet 106:411•422
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES IV (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286•289
Thorogood D, Kaiser WJ, Jones JG, Armstead I (2002) Self-incompatibility in ryegrass 12. Genotyping and mapping the S and Z loci of Lolium perenne L. Heredity 88:385•390
Tyler BF, Jones EL (1982) Evaluation of forage genetic resources in relation to breeding objectives and varietal assessment. In: Hayward MD (ed) The utilisation of genetic resources in fodder crop breeding. Proceedings of the Eucarpia fodder crops section meeting, Aberystwyth Institute for Grassland and Environmental Research (IGER), pp 148•162
Vance V, Vaucheret H (2001) RNA silencing in plants•defence and counterdefence. Science 292:2277•2280
Wilson ID, Barker GL, Edwards KJ (2003) Genotype to phenotype: a technological challenge. Ann Appl Bot 142:33•39
Yamada T, Jones ES, Nomura T, Hisano H, Shimamoto Y, Smith KF, Hayward MD, Forster JW (2004) QTL analysis of morphological, developmental and winter hardiness-associated traits in perennial ryegrass (Lolium perenne L.). Crop Sci 44:925•935
Zamir D, Tadmor Y (1986) Unequal segregation of nuclear genes in plants. Bot Gaz 147:355•358
Acknowledgements
We gratefully recognise technical support provided by Benjamin Franzmayr and Deborah Knox. The authors thank Prof. Michael Hayward for his careful critical reading of the manuscript. This work was performed within the Pasture Plant Genomics Program co-funded by the Department of Primary Industries, Victoria, Australia and AgResearch Limited, New Zealand. Funding was provided to AgResearch Ltd by the New Zealand Foundation for Research, Science and Technology under contract number C10X0203. Genetic mapping family development and genomic DNA-derived SSR genotyping was supported by the Molecular Plant Breeding Cooperative Research Centre (CRC). All experiments conducted during this study comply with current Australian laws.
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Communicated by G. Wenzel
An erratum to this article can be found at http://dx.doi.org/10.1007/s00122-005-1959-y
M.J. Faville and A.C. Vecchies contributed equally to this work.
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Faville, M.J., Vecchies, A.C., Schreiber, M. et al. Functionally associated molecular genetic marker map construction in perennial ryegrass (Lolium perenne L.). Theor Appl Genet 110, 12–32 (2004). https://doi.org/10.1007/s00122-004-1785-7
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DOI: https://doi.org/10.1007/s00122-004-1785-7