The Wheat Black Jack: Advances Towards Sequencing the 21 Chromosomes of Bread Wheat

  • Frédéric Choulet
  • Mario Caccamo
  • Jonathan Wright
  • Michael Alaux
  • Hana Šimková
  • Jan Šafář
  • Philippe Leroy
  • Jaroslav Doležel
  • Jane Rogers
  • Kellye Eversole
  • Catherine Feuillet
Chapter

Abstract

Despite its socio-economic importance and the overall recognition that a reference genome sequence has great value for crop improvement, sequencing the wheat genome has long been considered “impossible” because of the sequencing cost and bioinformatic challenges associated with the assembly of the mostly repetitive 17 Gb hexaploid genome. In the past 5 years, however, new platforms and technologies have emerged that enabled the launching of an international effort to tackle the bread wheat genome sequence using a chromosome-by-chromosome approach. In this chapter, we review the features of the wheat genome as well as the tools and technologies that can be used to sequence, assemble, and annotate a large, complex, polyploid genome. We describe the strategies and current status of the efforts towards achieving a reference sequence for the 21 chromosomes of bread wheat. Finally, we present the databases that were established to support the integration of the sequence information with other genetic and biological information.

Keywords

Wheat Polyploid Chromosome Flow sorting Physical map Genome sequence Next generation sequencing Assembly Annotation Transposable elements Database Data integration 

References

  1. AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  2. Akhunov ED, Akhunova AR, Dvorak J (2007) Mechanisms and rates of birth and death of dispersed duplicated genes during the evolution of a multigene family in diploid and tetraploid wheats. Mol Biol Evol 24:539–550PubMedCrossRefGoogle Scholar
  3. Amano N, Tanaka T, Numa H et al (2010) Efficient plant gene identification based on interspecies mapping of full-length cDNAs. DNA Res 17:271–279PubMedCentralPubMedCrossRefGoogle Scholar
  4. Astier Y, Braha O, Bayley H (2006) Toward single molecule DNA sequencing: Direct identification of ribonucleoside and deoxyribonucleoside 5 ’-monophosphates by using an engineered protein nanopore equipped with a molecular adapter. J Am Chem Soc 128:1705–1710PubMedCrossRefGoogle Scholar
  5. Bennett ST, Barnes C, Cox A et al (2005) Toward the $1000 human genome. Pharmacogenomics 6:373–382PubMedCrossRefGoogle Scholar
  6. Berkman P, Skarshewski A, Manoli S et al (2011a) Sequencing wheat chromosome arm 7BS delimits the 7BS/4AL translocation and reveals homoeologous gene conservation. Theor Appl Genet:1–10Google Scholar
  7. Berkman PJ, Skarshewski A, Lorenc MT et al (2011b) Sequencing and assembly of low copy and genic regions of isolated Triticum aestivum chromosome arm 7DS. Plant Biotech J 9:768–775CrossRefGoogle Scholar
  8. Brenchley R, Spannagl M, Pfeifer M, Barker GL, D'Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710Google Scholar
  9. Birney E, Stamatoyannopoulos JA, Dutta A et al (2007) Identification and analysis of functional elements in 1 % of the human genome by the ENCODE pilot project. Nature 447:799–816PubMedCrossRefGoogle Scholar
  10. Brisson N, Gate P, Gouache D et al (2010) Why are wheat yields stagnating in Europe? A comprehensive data analysis for France. Field Crop Res 119:201–212CrossRefGoogle Scholar
  11. Cantarel BL, Korf I, Robb SMC et al (2008) MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18:188–196PubMedCentralPubMedCrossRefGoogle Scholar
  12. Chaisson M, Pevzner P, Tang H (2004) Fragment assembly with short reads. Bioinformatics 20:2067–2074PubMedCrossRefGoogle Scholar
  13. Chantret N, Cenci A, Sabot F, Anderson O, Dubcovsky J (2004) Sequencing of the Triticum monococcum hardness locus reveals good microcolinearity with rice. Mol Genet Genomics 271:377–386PubMedCrossRefGoogle Scholar
  14. Charles M, Belcram H, Just J et al (2008) Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. Genetics 180:1071–1086PubMedCentralPubMedCrossRefGoogle Scholar
  15. Choulet F, Wicker T, Rustenholz C et al (2010) Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22:1686–1701PubMedCentralPubMedCrossRefGoogle Scholar
  16. Curwen V, Eyras E, Andrews TD et al (2004) The Ensembl automatic gene annotation system. Genome Res 14:942–950PubMedCentralPubMedCrossRefGoogle Scholar
  17. Devos KM, Ma J, Pontaroli AC et al (2005) Analysis and mapping of randomly chosen bacterial artificial chromosome clones from hexaploid bread wheat. Proc Natl Acad Sci U S A 102:19243–19248PubMedCentralPubMedCrossRefGoogle Scholar
  18. Dolezel J, Kubalakova M, Bartos J, Macas J (2004) Flow cytogenetics and plant genome mapping. Chromosome Res 12:77–91PubMedCrossRefGoogle Scholar
  19. Dolezel J, Kubalakova M, Paux E et al (2007) Chromosome-based genomics in the cereals. Chromosome Res 15:51–66PubMedCrossRefGoogle Scholar
  20. Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862–1866PubMedCrossRefGoogle Scholar
  21. Earl D, Bradnam K, JJ St (2011) Assemblathon 1: A competitive assessment of de novo short read assembly methods. Genome Res 21:2224–2241PubMedCentralPubMedCrossRefGoogle Scholar
  22. Eid J, Fehr A, Gray J et al (2009) Real-time DNA sequencing from single polymerase molecules. Science 323:133–138PubMedCrossRefGoogle Scholar
  23. Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307CrossRefGoogle Scholar
  24. Erayman M, Sandhu D, Sidhu D et al (2004) Demarcating the gene-rich regions of the wheat genome. Nucl Acids Res 32:3546–3565PubMedCentralPubMedCrossRefGoogle Scholar
  25. Estill JC, Bennetzen JL (2009) The DAWGPAWS pipeline for the annotation of genes and transposable elements in plant genomes. Plant Methods 5:8PubMedCentralPubMedCrossRefGoogle Scholar
  26. Feldman M, Levy AA (2009) Genome evolution in allopolyploid wheat–a revolutionary reprogramming followed by gradual changes. J Genet Genomics 36:511–518PubMedCrossRefGoogle Scholar
  27. Feuillet C, Eversole K (2007) Physical mapping of the wheat genome: A coordinated effort to lay the foundation for genome sequencing and develop tools for breeders. Isr J Plant Sci 55:307–313CrossRefGoogle Scholar
  28. Feuillet C, Keller B (1999) High gene density is conserved at syntenic loci of small and large grass genomes. Proc Natl Acad Sci. USA 96:8265–8270CrossRefGoogle Scholar
  29. Feuillet C, Salse J (2009) Comparative Genomics in the Triticeae. In: Feuillet C, Muehlbauer GJ (eds) Plant Genetics and Genomics. Springer, New York, pp 451–477Google Scholar
  30. Feuillet C, Leach JE, Rogers J et al (2011) Crop genome sequencing: lessons and rationales. Trends Plant Sci 16:77–88PubMedCrossRefGoogle Scholar
  31. Flavell RB, Rimpau J, Smith DB (1977) Repeated sequence DNA relationship in four cereals genomes. Chromosoma 63:205–222CrossRefGoogle Scholar
  32. Foley JA, Ramankutty N, Brauman KA et al (2011) Solutions for a cultivated planet. Nature 478:337–342PubMedCrossRefGoogle Scholar
  33. Gill KS, Gill BS, Endo TR, Boyko EV (1996a) Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics 143:1001–1012Google Scholar
  34. Gill KS, Gill BS, Endo TR, Taylor T (1996b) Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics 144:1883–1891Google Scholar
  35. Gill BS, Appels R, Botha-Oberholster A-M et al (2004) A Workshop Report on Wheat Genome Sequencing: International Genome Research on Wheat Consortium. Genetics 168:1087–1096PubMedCentralPubMedCrossRefGoogle Scholar
  36. Gnerre S, MacCallum I, Przybylski D et al (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci. USA 108:1513–1518CrossRefGoogle Scholar
  37. Havlak P, Chen R, Durbin KJ et al (2004) The Atlas genome assembly system. Genome Res 14:721–732PubMedCentralPubMedCrossRefGoogle Scholar
  38. Hernandez P, Martis M, Dorado G et al (2011) Next-generation sequencing and syntenic integration of flow-sorted arms of wheat chromosome 4A exposes the chromosome structure and gene content. The Plant J: 69:377–386.Google Scholar
  39. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  40. IRGSP IRGSP (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  41. Jaffe DB, Butler J, Gnerre S et al (2003) Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res 13:91–96PubMedCentralPubMedCrossRefGoogle Scholar
  42. Janda J, Bartoš J, Šafář J et al (2004) Construction of a subgenomic BAC library specific for chromosomes 1D, 4D and 6D of hexaploid wheat. Theor Appl Genet 109:1337–1345PubMedCrossRefGoogle Scholar
  43. Ling HQ, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, Lou X, Chen J, Feng M, Jian J, Zhang X, Luo G, Jiang Y, Liu J, Wang Z, Sha Y, Zhang B, Wu H, Tang D, Shen Q, Xue P, Zou S, Wang X, Liu X, Wang F, Yang Y, An X, Dong Z, Zhang K, Zhang X, Luo MC, Dvorak J, Tong Y, Wang J, Yang H, Li Z, Wang D, Zhang A, Wang J (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87–90Google Scholar
  44. Kubaláková M, Vrána J, Číhalíková J et al (2002) Flow karyotyping and chromosome sorting in bread wheat (Triticum aestivum L.). Theor Appl Genet 104:1362–1372PubMedCrossRefGoogle Scholar
  45. Kubaláková M, Kovářová P, Suchánková P et al (2005) Chromosome sorting in tetraploid wheat and its potential for genome analysis. Genetics 170:823–829PubMedCentralPubMedCrossRefGoogle Scholar
  46. La Rota M, Sorrells ME (2004) Comparative DNA sequence analysis of mapped wheat ESTs reveals the complexity of genome relationships between rice and wheat. Funct Integr Genomics 4:34–46PubMedCrossRefGoogle Scholar
  47. Lamoureux D, Peterson DG, Li W et al (2005) The efficacy of Cot-based gene enrichment in wheat (Triticum aestivum L.). Genome 48:1120–1126PubMedCrossRefGoogle Scholar
  48. Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedCrossRefGoogle Scholar
  49. Lenzerini M (2002) Data integration: a theoretical perspective. Proceedings of the twenty-first ACM SIGMOD-SIGACT-SIGART symposium on Principles of database systems. ACM. Wisconsin, Madison, pp 233–246Google Scholar
  50. Leroy P, Guilhot N, Sakai H et al (2012) TriAnnot: a versatile and high performance pipeline for the automated annotation of plant genomes. Frontiers in Plant Sciences 3:1–14Google Scholar
  51. Li W, Gill B (2004) Genomics for cereal improvement. In: Gupta PK, Varshney RK (eds) Cereal genomics. Kluwer Academic Publishers, Dordrecht, pp 585–634Google Scholar
  52. Li W, Zhang P, Fellers JP et al (2004) Sequence composition, organization, and evolution of the core Triticeae genome. Plant J 40:500–511PubMedCrossRefGoogle Scholar
  53. Li R, Yu C, Li Y et al (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967PubMedCrossRefGoogle Scholar
  54. Liang C, Mao L, Ware D, Stein L (2009) Evidence-based gene predictions in plant genomes. Genome Res 19:1912–1923PubMedCentralPubMedCrossRefGoogle Scholar
  55. Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer KF, Li D, Pan S,Zheng F, Hu Q, Xia X, Li J, Liang Q, Chen J, Wicker T, Gou C, Kuang H, He G, Luo Y, Keller B, Xia Q, Lu P, Wang J, Zou H, Zhang R, Xu J, Gao J, Middleton C,Quan Z, Liu G, Wang J; International Wheat Genome Sequencing Consortium, Yang H, Liu X, He Z, Mao L, Wang J (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95Google Scholar
  56. Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate Trends and Global Crop Production Since 1980. Science DOI:10.1126/science.1204531Google Scholar
  57. Margulies M, Egholm M, Altman WE et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedCentralPubMedGoogle Scholar
  58. Massa AN, Wanjugi H, Deal KR et al (2011) Gene Space Dynamics During the Evolution of Aegilops tauschii, Brachypodium distachyon, Oryza sativa, and Sorghum bicolor Genomes. Mol Biol Evol 28:2537–2547PubMedCentralPubMedCrossRefGoogle Scholar
  59. Mayer KF, Taudien S, Martis M et al (2009) Gene content and virtual gene order of barley chromosome 1H. Plant Physiol 151:496–505PubMedCentralPubMedCrossRefGoogle Scholar
  60. Mayer KF, Martis M, Hedley PE et al (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263PubMedCentralPubMedCrossRefGoogle Scholar
  61. McFadden E, Sears E (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J Hered 37:81–89107PubMedGoogle Scholar
  62. Metzker ML (2009) Sequencing technologies – the next generation. Nat Rev Genet 11:31–46PubMedCrossRefGoogle Scholar
  63. Muniz LM, Cuadrado A, Jouve N, Gonzalez JM (2001) The detection, cloning, and characterisation of WIS 2–1A retrotransposon-like sequences in Triticum aestivum L. and xTriticosecale Wittmack and an examination of their evolution in related Triticeae. Genome 44:979–989PubMedCrossRefGoogle Scholar
  64. Ouyang S, Buell CR (2004) The TIGR Plant Repeat Databases: a collective resource for the identification of repetitive sequences in plants. Nucleic Acids Res 32:D360–363Google Scholar
  65. Parkhill J, Birney E, Kersey P (2010) Genomic information infrastructure after the deluge. Genome Biol 11:402PubMedCentralPubMedCrossRefGoogle Scholar
  66. Paux E, Roger D, Badaeva E et al (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
  67. Paux E, Sourdille P, Salse J et al (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104PubMedCrossRefGoogle Scholar
  68. Paux E, Sourdille P, Mackay I, Feuillet C (2011) Sequence-based marker development in wheat: Advances and applications to breeding. Biotechnol Adv 30:1071–1088PubMedCrossRefGoogle Scholar
  69. Pevzner PA, Tang H, Waterman MS (2001) An Eulerian path approach to DNA fragment assembly. Proc Natl Acad Sci U S A 98:9748–9753PubMedCentralPubMedCrossRefGoogle Scholar
  70. Qi LL, Echalier B, Chao S et al (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712PubMedCentralPubMedCrossRefGoogle Scholar
  71. Rabinowicz PD, Citek R, Budiman MA et al (2005) Differential methylation of genes and repeats in land plants. Genome Res 15:1431–1440PubMedCentralPubMedCrossRefGoogle Scholar
  72. Rounsley S, Marri P, Yu Y et al (2009) De Novo Next Generation Sequencing of Plant Genomes. Rice 2:35–43CrossRefGoogle Scholar
  73. Rustenholz C, Choulet F, Laugier C et al (2011) A 3000-loci transcription map of chromosome 3B unravels the structural and functional features of gene islands in hexaploid wheat. Plant Physiol 157:1596–1608PubMedCentralPubMedCrossRefGoogle Scholar
  74. Sabot F, Guyot R, Wicker T et al (2005) Updating of transposable element annotations from large wheat genomic sequences reveals diverse activities and gene associations. Mol Genet Genomics 274:119–130PubMedCrossRefGoogle Scholar
  75. Šafář J, Bartoš J, Janda J et al (2004) Dissecting large and complex genomes: flow sorting and BAC cloning of individual chromosomes from bread wheat. Plant J 39:960–968PubMedCrossRefGoogle Scholar
  76. Šafář J, Šimková H, Kubaláková M et al (2010) Development of chromosome-specific BAC resources for genomics of bread wheat. Cytogenet Genome Res 129:211–223PubMedCrossRefGoogle Scholar
  77. Sakata K, Nagamura Y, Numa H et al (2002) RiceGAAS: an automated annotation system and database for rice genome sequence. Nucleic Acids Res 30:98–102PubMedCentralPubMedCrossRefGoogle Scholar
  78. Sandhu D, Gill KS (2002) Gene-Containing Regions of Wheat and the Other Grass Genomes. Plant Physiol 128:803–811PubMedCentralPubMedCrossRefGoogle Scholar
  79. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci of the United States of America 74:5463–5467Google Scholar
  80. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115PubMedCrossRefGoogle Scholar
  81. Sears ER (1954) The aneuploid of common wheat. Mo Agr Exp Sta Res Bull 572:1–58Google Scholar
  82. Sears ER, Sears L (1978) The telocentric chromosomes of common wheat In: Ramanujams S (ed) Proc 5th Int Wheat Genetics Symp. Indian Agricultural Research Institute, New Delhi, India. , pp 389–407Google Scholar
  83. Simkova H, Svensson JT, Condamine P et al (2008) Coupling amplified DNA from flow-sorted chromosomes to high-density SNP mapping in barley. BMC Genomics 9:294PubMedCentralPubMedCrossRefGoogle Scholar
  84. Simpson JT, Durbin R (2010) Efficient construction of an assembly string graph using the FM-index. Bioinformatics 26:i367–i373Google Scholar
  85. Simpson JT, Wong K, Jackman SD et al (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123PubMedCentralPubMedCrossRefGoogle Scholar
  86. Smith DB, Flavell RB (1975) Characterization of Wheat Genome by Renaturation Kinetics. Chromosoma 50:223–242CrossRefGoogle Scholar
  87. Sorrells ME, La Rota M, Bermudez-Kandianis CE et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827PubMedCentralPubMedGoogle Scholar
  88. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–814CrossRefGoogle Scholar
  89. Valouev A, Ichikawa J, Tonthat T et al (2008) A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res 18:1051–1063PubMedCentralPubMedCrossRefGoogle Scholar
  90. Venter JC, Adams MD, Myers EW et al (2001) The Sequence of the Human Genome. Science 291:1304–1351PubMedCrossRefGoogle Scholar
  91. Vitulo N, Albiero A, Forcato C et al (2011) First survey of the wheat chromosome 5A composition through a Next Generation Sequencing approach. PLoS ONE 6:e26421PubMedCentralPubMedCrossRefGoogle Scholar
  92. Vrána J, Kubaláková M, Šimková H et al (2000) Flow sorting of mitotic chromosomes in common wheat (Triticum aestivum L.). Genetics 156:2033–2041PubMedCentralPubMedGoogle Scholar
  93. Waterston RH, Lindblad-Toh K, Birney E et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562PubMedCrossRefGoogle Scholar
  94. Wei F, Zhang J, Zhou S et al (2009) The physical and genetic framework of the maize B73 genome. PLoS Genet 5:e1000715PubMedCentralPubMedCrossRefGoogle Scholar
  95. Wicker T, Stein N, Albar L et al (2001) Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J 26:307–316PubMedCrossRefGoogle Scholar
  96. Wicker T, Matthews DE, Keller B (2002) TREP: a database for Triticeae repetitive elements. Trends Plant Sci 7:561–562CrossRefGoogle Scholar
  97. Wicker T, Mayer KFX, Gundlach H et al (2011) Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives. Plant Cell 23:1706–18PubMedCentralPubMedCrossRefGoogle Scholar
  98. Yan L, Loukoianov A, Tranquilli G et al (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268PubMedCentralPubMedCrossRefGoogle Scholar
  99. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829PubMedCentralPubMedCrossRefGoogle Scholar
  100. Zhou S, Bechner M, Place M et al (2007) Validation of rice genome sequence by optical mapping. BMC Genomics 8:278PubMedCentralPubMedCrossRefGoogle Scholar
  101. Zohary D, Hopf M (2000) Domestication of plants in the old world, 3rd edn. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Frédéric Choulet
    • 1
    • 2
  • Mario Caccamo
    • 3
  • Jonathan Wright
    • 3
  • Michael Alaux
    • 4
  • Hana Šimková
    • 5
  • Jan Šafář
    • 5
  • Philippe Leroy
    • 1
    • 2
  • Jaroslav Doležel
    • 5
  • Jane Rogers
    • 3
  • Kellye Eversole
    • 6
  • Catherine Feuillet
    • 1
    • 2
  1. 1.Genetics, Diversity and Ecophysiology of CerealsINRA Joint Research Unit 1095 GeneticsClermont-FerrandFrance
  2. 2.Genetics, Diversity and Ecophysiology of CerealsUniversity Blaise Pascal Joint Research Unit 1095 GeneticsClermont-FerrandFrance
  3. 3.The Genome Analysis Centre, Norwich Research ParkColneyUK
  4. 4.INRA Centre de Versailles-GrignonUnité de Recherche en Génomique-InfoVersaillesFrance
  5. 5.Centre of the Region Haná for Biotechnological and Agricultural ResearchInstitute of Experimental BotanyOlomoucCzech Republic
  6. 6.International Wheat Genome Sequencing ConsortiumEversole AssociatesBethesdaUSA

Personalised recommendations