Theoretical and Applied Genetics

, Volume 123, Issue 4, pp 555–569 | Cite as

High-throughput SNP discovery and genotyping in durum wheat (Triticum durum Desf.)

  • Daniele Trebbi
  • Marco Maccaferri
  • Peter de Heer
  • Anker Sørensen
  • Silvia Giuliani
  • Silvio Salvi
  • Maria Corinna Sanguineti
  • Andrea Massi
  • Edwin Andries Gerard van der Vossen
  • Roberto Tuberosa
Original Paper

Abstract

We describe the application of complexity reduction of polymorphic sequences (CRoPS®) technology for the discovery of SNP markers in tetraploid durum wheat (Triticum durum Desf.). A next-generation sequencing experiment was carried out on reduced representation libraries obtained from four durum cultivars. SNP validation and minor allele frequency (MAF) estimate were carried out on a panel of 12 cultivars, and the feasibility of genotyping these SNPs in segregating populations was tested using the Illumina Golden Gate (GG) technology. A total of 2,659 SNPs were identified on 1,206 consensus sequences. Among the 768 SNPs that were chosen irrespective of their genomic repetitiveness level and assayed on the Illumina BeadExpress genotyping system, 275 (35.8%) SNPs matched the expected genotypes observed in the SNP discovery phase. MAF data indicated that the overall SNP informativeness was high: a total of 196 (71.3%) SNPs had MAF >0.2, of which 76 (27.6%) showed MAF >0.4. Of these SNPs, 157 were mapped in one of two mapping populations (Meridiano × Claudio and Colosseo × Lloyd) and integrated into a common genetic map. Despite the relatively low genotyping efficiency of the GG assay, the validated CRoPS-derived SNPs showed valuable features for genomics and breeding applications such as a uniform distribution across the wheat genome, a prevailing single-locus codominant nature and a high polymorphism. Here, we report a new set of 275 highly robust genome-wide Triticum SNPs that are readily available for breeding purposes.

Supplementary material

122_2011_1607_MOESM1_ESM.ods (119 kb)
Online Resource 1 Details of the 768 SNP-harboring sequences selected for the two OPA assays. A = Keygene and University of Bologna (KBO) SNP name B = Nucleotide identified during the CRoPS analysis. Dots indicate insufficient number of sequence to identify nucleotides C = Genotype identified during the Golden Gate (GG) assay. Scores A, B, H and U indicate homozygosity for the first allele, homozygosity for the second allele, heterozygosity and undetermined genotype, respectively (ODS 118 kb)

References

  1. Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141PubMedCrossRefGoogle Scholar
  2. Akbari M, Wenzl P, Caig V, Carling J, Xia L, Yang SY, Uszynski G, Mohler V, Lehmensiek A, Kuchel H, HM J, Howes N, Sharp P, Vaughan P, Rathmell B, Huttner E, Kilian A (2006) Diversity array technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet 113:1409–1420PubMedCrossRefGoogle Scholar
  3. Akhunov ED, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the illumina Golden Gate assay. Theor Appl Genet 119:507–517PubMedCrossRefGoogle Scholar
  4. Akhunov ED, Akhunova AR, Anderson OD, Anderson JA, Blake N, Clegg MT, Coleman-Derr D, Conley EJ, Crossman CC, Deal KR, Dubcovsky J, Gill BS, Gu YQ, Hadam J, Heo H, Huo N, Lazo GR, Luo MC, Ma YQ, Matthews DE, McGuire PE, Morrell PL, Qualset CO, Renfro J, Tabanao D, Talbert LE, Tian C, Toleno DM, Warburton ML, You FM, Zhang W, Dvorak J (2010) Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes. BMC Genomics 11:702PubMedCrossRefGoogle Scholar
  5. Albert TJ, Molla MN, Muzny DM, Nazareth L, Wheeler D, Song X, Richmond TA, Middle C, Rodesch MJ, Packard CJ, Weinstock GM, Gibbs RA (2007) Direct selection of human genomic loci by microarray hybridization. Nat Methods 4:903–905PubMedCrossRefGoogle Scholar
  6. Altshuler D, Pollara VJ, Cowles CR, van Etten WJ, Baldwin J, Linton L, Lander ES (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516PubMedCrossRefGoogle Scholar
  7. Barbazuk WB, Emrich SJ, Chen HD, Li L, Schnable PS (2007) SNP discovery via 454 transcriptome sequencing. Plant J 51:910–918PubMedCrossRefGoogle Scholar
  8. Barker GLA, Edwards KJ (2009) A genome-wide analysis of single nucleotide polymorphism diversity in the world’s major cereal crops. Plant Biotechnol J 7:318–325PubMedCrossRefGoogle Scholar
  9. Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132PubMedCrossRefGoogle Scholar
  10. Brookes AJ (1999) The essence of SNPs. Gene 234:177–186PubMedCrossRefGoogle Scholar
  11. Chao S, Dubcovsky J, Dvorak J, Luo MC, Baenziger SP, Matnyazov R, Clark DR, Talbert LE, Anderson JA, Dreisigacker S, Glover K, Chen J, Campbell K, Bruckner PL, Rudd JC, Haley S, Carver BF, Perry S, Sorrells ME, Akhunov ED (2010) Population- and genome-specific patterns of linkage disequilibrium and SNP variation in spring and winter wheat (Triticum aestivum L.). BMC Genomics 11:727PubMedCrossRefGoogle Scholar
  12. Chen X, Levine L, Kwok PY (1999) Fluorescence polarization in homogeneous nucleic acid analysis. Genome Res 9:492–498PubMedGoogle Scholar
  13. Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3:19PubMedCrossRefGoogle Scholar
  14. Close T, Bhat P, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson J, Wanamaker S, Bozdag S, Roose M, Moscou M, Chao S, Varshney R, Szucs P, Sato K, Hayes P, Matthews D, Kleinhofs A, Muehlbauer G, DeYoung J, Marshall D, Madishetty K, Fenton R, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10:582PubMedCrossRefGoogle Scholar
  15. Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B: J Biol Sci 363:557–572CrossRefGoogle Scholar
  16. de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) Carthagene: multipopulation integrated genetic and radiation hybrid mapping. Bioinformatics 21:1703–1704PubMedCrossRefGoogle Scholar
  17. Deschamps S, Campbell M (2010) Utilization of next-generation sequencing platforms in plant genomics and genetic variant discovery. Mol Breed 25:553–570CrossRefGoogle Scholar
  18. Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid whet under domestication. Science 316:1862–1866PubMedCrossRefGoogle Scholar
  19. Edwards D, Batley J (2010) Plant genome sequencing: applications for crop improvement. Plant Biotechnol J 8:2–9PubMedCrossRefGoogle Scholar
  20. Edwards KJ, Poole RL, Barker GLA (2008) SNP discovery in plants. In: Henry RJ (ed) Plant genotyping II: SNP Technology. Wallingford, Oxfordshire, pp 1–29Google Scholar
  21. Fan JB, Oliphant A, Shen R, Kermani BG, Garcia F, Gunderson KL, Hansen M, Steemers F, Butler SL, Deloukas P, Galver L, Hunt S, McBride C, Bibikova M, Rubano T, Chen J, Wickham E, Doucet D, Wang W, Campbell D, Zhang B, Kruglyak S, Bentley D, Haas J, Rigault P, Zhou L, Stuelpnagel J, Chee MS (2003) High parallel SNP genotyping. Cold Spring Harb Symp Quant Biol 68:69–78PubMedCrossRefGoogle Scholar
  22. Feltus FA, Wasn J, Schulze SR, Estill JC, Jiang N, Paterson AH (2004) An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments. Genome Res 14:1812–1819PubMedCrossRefGoogle Scholar
  23. Flavell RB, Rimpau J, Smith DB (1977) Repeated sequence DNA relationships in four cereal genomes. Chromosoma 63:205–222CrossRefGoogle Scholar
  24. Ganal MW, Röder MS (2007) Microsatellite and SNP markers in wheat breeding. In: Varshney RK, Tuberosa R (eds) Genomics-assisted crop improvement, vol 2: genomics applications in crops. Springer, New York, pp 1–24Google Scholar
  25. Ganal MW, Altmann T, Röder MS (2009) SNP identification in crop plants. Curr Opin Plant Biol 12:211–217PubMedCrossRefGoogle Scholar
  26. Gunderson KL (2009) Whole-genome genotyping on bead arrays. Methods Mol Biol 529:197–213PubMedCrossRefGoogle Scholar
  27. Gut IG (2001) Automation in genotyping of single nucleotide polymorphisms. Hum Mutat 17:475–492PubMedCrossRefGoogle Scholar
  28. Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C, Hochu I, Poirier S, Santoni S, Glemin S, David J (2007) Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol 24:1506–1517PubMedCrossRefGoogle Scholar
  29. Hayden MJ, Tabone TL, Nguyen TM, Coventry S, Keiper FJ, Fox RL, Chalmers KJ, Mather DE, Eglinton JK (2009) An informative set of SNP markers for molecular characterisation of Australian barley germplasm. Crop Pasture Sci 61:70–83CrossRefGoogle Scholar
  30. Huang X, Feng Q, Qian Q, Zhao Q, Wang L, Wang A, Guan J, Fan D, Weng Q, Huang T, Dong G, Sang T, Han B (2009) High-throughput genotyping by whole-genome resequencing. Genome Res 19:1068–1076PubMedCrossRefGoogle Scholar
  31. Hyten DL, Song Q, Choi IY, Yoon MS, Specht JE, Matukumalli LK, Nelson RL, Shoemaker RC, Young ND, Cregan PB (2008) High-throughput genotyping with the Golden Gate assay in the complex genome of soybean. Theor Appl Genet 116:945–952PubMedCrossRefGoogle Scholar
  32. Hyten DL, Cannon SB, Song Q, Weeks N, Fickus EW, Shoemaker RC, Specht JE, Farmer AD, May GD, Cregan PB (2010) High-throughput SNP discovery through deep resequencing of a reduced representation library to anchor and orient scaffolds in the soybean whole genome sequence. BMC Genomics 11:38PubMedCrossRefGoogle Scholar
  33. Jander G, Norris SR, Rounsley SD, Bush DF, Levin IM, Last RL (2002) Arabidopsis map-based cloning in the post-genome era. Plant Physiol 129:440–450PubMedCrossRefGoogle Scholar
  34. Jannink J, Lorenz AJ (2010) Genomic selection in plant breeding: from theory to practice. Brief Funct Genomics 9:166–177PubMedCrossRefGoogle Scholar
  35. Jones E, Chu WC, Ayele M, Ho J, Bruggeman E, Yourstone K, Rafalski A, Smith OS, McMullen M, Bezawada C, Warren J, Babayev J, Basu S, Smith S (2009) Development of single nucleotide polymorphism (SNP) markers for use in commercial maze (Zea mays L.) germplasm. Mol Breed 24:165–176CrossRefGoogle Scholar
  36. Koebner R, Summers R (2002) The impact of molecular markers on the wheat breeding paradigm. Cell Mol Biol Lett 7:695–702PubMedGoogle Scholar
  37. Korzun V, Röder M, Wendehake K, Pasqualone A, Lotti C, Ganal M, Blanco A (1999) Integration of dinucleotide microsatellites from hexaploid bread wheat into a genetic linkage map of durum wheat. Theor Appl Genet 98:1202–1207CrossRefGoogle Scholar
  38. Liu S, Chen HD, Makarevitch I, Shirmer R, Emrich SJ, Dietrich CR, Barbazuk WB, Springer NM, Schnable PS (2010) High-throughput genetic mapping of mutants via quantitative single nucleotide polymorphism typing. Genetics 184:19–26PubMedCrossRefGoogle Scholar
  39. Livak KJ, Flood SJ, Marmaro J, Giusti W, Deetz K (1995) Oligonucleotide with fluorescent dyes at opposite ends provide a quenched probe system useful for detecting PCR product and nucleic acid hybridization. Genome Res 4:357–362CrossRefGoogle Scholar
  40. Lotti C, Salvi S, Pasqualone A, Tuberosa R, Blanco A (2000) Integration of AFLP markers into an RFLP-based map of durum wheat. Plant Breed 119:393–401CrossRefGoogle Scholar
  41. Maccaferri M, Sanguineti MC, Noli E, Tuberosa R (2005) Population structure and long-range linkage disequilibrium in a durum wheat elite collection. Mol Breed 15:271–290CrossRefGoogle Scholar
  42. Maccaferri M, Sanguineti MC, Natoli V, Araus Ortega JL, Ben Salem M, Bort J, Chenenaoui S, De Ambrogio E, Garci’a del Moral L, Demontis A, El-Ahmed A, Maalouf F, Machlab H, Moragues M, Motawaj J, Nachit M, Nserallh N, Ouabbou H, Royo C, Tuberosa R (2006) A panel of elite accessions of durum wheat (Triticum durum Desf.) suitable for association mapping studies. Plant Genet Resour 4:79–85CrossRefGoogle Scholar
  43. Maccaferri M, Mantovani P, Tuberosa R, Deambrogio E, Giuliani S, Demontis A, Massi A, Sanguineti MC (2008) A major QTL for durable leaf rust resistance widely exploited in durum wheat breeding programs maps on the distal region of chromosome arm 7BL. Theor Appl Genet 117:1225–1240PubMedCrossRefGoogle Scholar
  44. Maccaferri M, Sanguineti MC, Demontis A, El-Ahmed A, Garcia del Moral L, Maalouf F, Nachit M, Nserallah N, Ouabbou H, Rhouma S, Royo C, Villegas D, Tuberosa R (2011) Association mapping in durum wheat grown across a broad range of water regimes. J Exp Bot 62:409–438Google Scholar
  45. Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12:57–63Google Scholar
  46. Mammadov JA, Chen W, Ren R, Pai R, Marchione W, Yalcin F, Witsenboer H, Greene TW, Thompson SA, Kumpatla SP (2010) Development of highly polymorphic SNP markers from the complexity reduced portion of maize (Zea mays L.) genome for use in marker-assisted breeding. Theor Appl Genet 121:577–588PubMedCrossRefGoogle Scholar
  47. Mantovani P, Maccaferri M, Sanguineti MC, Tuberosa R, Catizone I, Wenzl P, Thomson B, Carling J, Huttner E, DeAmbrogio E, Kilian A (2008) An integrated DArT–SSR linkage map of durum wheat. Mol Breed 22:629–648CrossRefGoogle Scholar
  48. McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, Ulat VJ, Zeller G, Clark RM, Hoen DR, Bureau TE, Stokowski R, Ballinger DG, Frazer KA, Cox DR, Padhukasahasram B, Bustamante CD, Weigel D, Mackill DJ, Bruskiewich RM, Rãtsch G, Buell CR, Leung H, Leach JE (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci USA 106:12273–12278PubMedCrossRefGoogle Scholar
  49. Nijman IJ, Kuipers S, Verheul M, Guryev V, Cuppen E (2008) A genome-wide SNP panel for mapping and associations studies in the rat. BMC Genomics 9:95PubMedCrossRefGoogle Scholar
  50. Okou DT, Steinberg KM, Middle C, Cutler DJ, Albeert TJ, Zwick ME (2007) Microarray-based genomic selection for high-throughput resequencing. Nat Methods 4:907–909PubMedCrossRefGoogle Scholar
  51. Oliphant A, Barker DL, Stuelpnagel JR, Chee MS (2002) BeadArray technology: enabling an accurate, cost-effective approach to high-throughput genotyping. Biotechniques 32:S56–S61Google Scholar
  52. Olivier M (2005) The Invader assay for SNP genotyping. Mutat Res 573:103–110PubMedGoogle Scholar
  53. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D (2008) Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 18:2024–2033PubMedCrossRefGoogle Scholar
  54. Palmer LE, Rabinowicz PD, O’Shaughnessy A, Balija VLN, Dike S, de la Bastide M, Martienssen RA, McCombie WR (2003) Maize genome sequencing by methylation filtration. Science 302:2115–2117PubMedCrossRefGoogle Scholar
  55. Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C (2006) Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J 48:463–474PubMedCrossRefGoogle Scholar
  56. Peleg Z, Saranga Y, Suprunova T, Ronin Y, Röder M, Kilian A, Korol A, Fahima T (2008) High-density genetic map of durum wheat × wild emmer wheat based on SSR and DArT markers. Theor Appl Genet 117:103–115PubMedCrossRefGoogle Scholar
  57. Quraishi U, Abrouk M, Bolot S, Pont C, Throude M, Guilhot N, Confolent C, Bortolini F, Praud S, Murigneux A, Charmet G, Salse J (2010) Genomics in cereals: from genome-wide conserved orthologous set (COS) sequences to candidate genes for trait dissection. Funct Integr Genomics 9:473–484CrossRefGoogle Scholar
  58. Rafalski A (2002) Novel genetic mapping tools in plant: SNPs and LD-based approaches. Plant Sci 162:329–333CrossRefGoogle Scholar
  59. Ravel C, Praud S, Murigneux A, Canaguier A, Sapet F, Samson D, Balfourier F, Dufour P, Chalhoub B, Brunel D, Beckert M, Charmet G (2006) Single-nucleotide polymorphisms (SNPs) frequency in a set of selected lines of bread wheat (Triticum aestivum L.). Genome 49:1131–1139PubMedCrossRefGoogle Scholar
  60. Ravel C, Praud S, Canaguier A, Dufour P, Giancola S, Balfourier F, Chalhoub B, Brunel D, Linossier L, Dardevet M, Beckert M, Rousset M, Murigneux A, Charmet G (2007) DNA sequence polymorphisms and their application to bread wheat quality. Euphytica 158:331–336CrossRefGoogle Scholar
  61. Salvi S, Tuberosa R, Phillips RL (2001) Development of PCR-based assays for allelic discrimination in maize by using the 5′-nuclease procedure. Mol Breed 8:169–176CrossRefGoogle Scholar
  62. Sanchez J, Borsting C, Hallenberg C, Buchard A, Hernandez A, Morling N (2003) Multiplex PCR and minisequencing of SNPs—a model with 35 Y chromosome SNPs. Forensic Sci Int 137:74–84PubMedCrossRefGoogle Scholar
  63. Sandve SR, Rudi H, Dørum G, Vigeland MD, Berg PR, Rognli OA (2010) Genotyping unknown genomic terrain in complex plant genomes. In: Huyghe C (ed) Sustainable use of genetic diversity in forage and turf breeding. Springer, New Mexico, pp 455–459CrossRefGoogle Scholar
  64. Schnurbusch T, Collins NC, Eastwood RF, Sutton T, Jefferies SP, Langridge P (2007) Fine mapping and targeted SNP survey using rice-wheat gene colinearity in the region of the Bo1 boron toxicity tolerance locus of bread wheat. Theor Appl Genet 115:451–461PubMedCrossRefGoogle Scholar
  65. Shen R, Fan JB, Campbell D, Chang W, Chen J, Doucet D, Yeakley J, Bibikova M, Garcia EW, McBride C, Steemers F, Garcia F, Kermani BG, Gunderson K, Oliphant A (2005) High-throughput SNP genotyping on universal bead arrays. Mutat Res 573:70–82PubMedGoogle Scholar
  66. Shendure J, Li H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145PubMedCrossRefGoogle Scholar
  67. Somers DJ, Kirkpartick R, Moniwa M, Walsh A (2003) Mining single-nucleotide polymorphisms from hexaploid wheat ESTs. Genome 46:431–437PubMedCrossRefGoogle Scholar
  68. Song QJ, Shi JR, Singh S, Fickus EW, Costa JM, Lewis J, GB S, Ward R, Cregan PB (2005) Development and mapping of microsatellite (SSR) markers in wheat. Theor Appl Genet 110:550–560PubMedCrossRefGoogle Scholar
  69. van Eijk MJT, van der Poel (2006) Strategies for high throughput identification and detection of polymorphisms WO2006137733Google Scholar
  70. Van Ooijen JW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V., WageningenGoogle Scholar
  71. van Orsouw NJ, Hogers RCJ, Janssen A, Yalcin F, Snoeijers S, Verstege E, Schneiders H, van der Poel H, van Oeveren J, Verstegen H, van Eijk MJT (2007) Complexity reduction of polymorphic sequences (CRoPS): a novel approach for large-scale polymorphism discovery in complex genomes. PLoS One 2:e1172PubMedCrossRefGoogle Scholar
  72. Van Tassel PC, Smith TPL, Matukumalli LK, Taylor JF, Schnabel RD, Lawley CT, Haudenschild CD, Moore SS, Warren WC, Sonstegard TS (2008) SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries. Nat Methods 5:247–252CrossRefGoogle Scholar
  73. Varshney RK, Spurthi N, Nayak S, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530PubMedCrossRefGoogle Scholar
  74. Varshney RK, Glaszmann JC, Leung H, Ribaut JM (2010) More genomic resources for less-studied crops. Trends Biotechnol 28:452–460PubMedCrossRefGoogle Scholar
  75. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  76. Vuylsteke M, Mank R, Antonise R, Bastiaans E, Senior ML, Stuber CW, Melchinger AE, Lubberstedt T, Xia XC, Stam P, Zabeau M, Kuiper M (1999) Two high-density AFLP linkage maps of Zea mays L.: analysis of distribution of AFLP markers. Theor Appl Genet 99:921–935CrossRefGoogle Scholar
  77. Waugh R, Jannink J, Muehlbauer GJ, Ramsay L (2009) The emergence of whole genome association scans in barley. Curr Opin Plant Biol 12:218–222PubMedCrossRefGoogle Scholar
  78. Wenzl P, Li H, Carling J, Zhou M, Raman H, Paul E, Hearnden P, Maier C, Xia L, Caig V, Ovesná J, Cakir M, Poulsen D, Wang J, Raman R, Smith KP, Muehlbauer GJ, Chalmers KJ, Kleinhofs A, Huttner E, Kilian A (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics 7:206PubMedCrossRefGoogle Scholar
  79. Wright WT, Heggarty SV, Young IS, Nicholls DP, Whittall R, Humphries SE, Graham CA (2008) Multiplex MassARRAY spectrometry (iPLEX) produces a fast and economical test for 56 familial hypercholesterolaemia-causing mutations. Clin Genet 74:463–468PubMedCrossRefGoogle Scholar
  80. Yamamoto T, Nagasaki H, Yonemaru J, Ebana K, Nakajima M, Shibaya T, Yano M (2010) Fine definition of the pedigree haplotypes of closely related rice cultivars by means of genome-wide discovery of single-nucleotide polymorphisms. BMC Genomics 11:267PubMedCrossRefGoogle Scholar
  81. Yan J, Yang X, Shah T, Sánchez-Villeda H, Li J, Warburton M, Zhou Y, Crouch J, Xu Y (2010) High-throughput SNP genotyping with the Golden Gate assay in maize. Mol Breed 25:441–451CrossRefGoogle Scholar
  82. Yuan Y, SanMiguel PJ, Bennetzen JL (2003) High-Cot sequence analysis of the maize genome. Plant J 34:249–255PubMedCrossRefGoogle Scholar
  83. Zhang X, Borevitz JO (2009) Global analysis of allele-specific expression in Arabidopsis thaliana. Genetics 182:943–954PubMedCrossRefGoogle Scholar
  84. Zhao W, Canaran P, Jurkuta R, Fulton T, Glaubitz J, Buckler ES, Doebley J, Gaut B, Goodman M, Holland J, Kresovich S, McMullen M, Stein L, Ware D (2006) Panzea: a database and resource for molecular and functional diversity in the maize genome. Nucleic Acids Res 34:D752–D757PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Daniele Trebbi
    • 1
    • 4
  • Marco Maccaferri
    • 2
  • Peter de Heer
    • 1
  • Anker Sørensen
    • 1
  • Silvia Giuliani
    • 2
  • Silvio Salvi
    • 2
  • Maria Corinna Sanguineti
    • 2
  • Andrea Massi
    • 3
  • Edwin Andries Gerard van der Vossen
    • 1
  • Roberto Tuberosa
    • 2
  1. 1.Keygene N.V., Applied ResearchWageningenThe Netherlands
  2. 2.Dipartimento di Scienze e Tecnologie Agroambientali (DiSTA)Università di BolognaBolognaItaly
  3. 3.Società Produttori Sementi Bologna SpaArgelatoItaly
  4. 4.Dipartimento di Biotecnologie AgrarieUniversità degli Studi di PadovaLegnaroItaly

Personalised recommendations