Functional & Integrative Genomics

, Volume 9, Issue 1, pp 67–79 | Cite as

Structure–function analysis of the barley genome: the gene-rich region of chromosome 2HL

  • Andrew Chen
  • Anita Brûlé-Babel
  • Ute Baumann
  • Nicholas C. Collins
Original Paper

Abstract

A major gene-rich region on the end of the long arm of Triticeae group 2 chromosomes exhibits high recombination frequencies, making it an attractive region for positional cloning. Traits known to be controlled by this region include chasmogamy/cleistogamy, frost tolerance at flowering, grain yield, head architecture, and resistance to Fusarium head blight and rusts. To assist these cloning efforts, we constructed detailed genetic maps of barley chromosome 2H, including 61 polymerase chain reaction markers. Colinearity with rice occurred in eight distinct blocks, including five blocks in the terminal gene-rich region. Alignment of rice sequences from the junctions of colinear chromosome segments provided no evidence for the involvement of long (>2.5 kb) inverted repeats in generating inversions. However, reuse of some junction sequences in two or three separate evolutionary breakage/fusion events was implicated, suggesting the presence of fragile sites. Sequencing across 91 gene fragments totaling 107 kb from four barley genotypes revealed the highest single nucleotide substitution and insertion–deletion polymorphism levels in the terminal regions of the chromosome arms. The maps will assist in the isolation of genes from the chromosome 2L gene-rich region in barley and wheat by providing markers and accelerating the identification of the corresponding points in the rice genome sequence.

Keywords

Barley Sequence polymorphism Chromosome evolution 2H 

Supplementary material

10142_2008_99_MOESM1_ESM.pdf (199 kb)
Supplemental Table 1Primers, PCR conditions, restriction enzymes, and sequences relating to polymorphism screen and markers (PDF 199 KB).
10142_2008_99_Fig1_ESM.gif (41 kb)
Supplemental Fig. 1

Rearrangements of chromosome segments 2, 3, and 4 involve reuse of junction intervals A, B, C, or D in multiple chromosome breakage/fusion events. The six possible scenarios in regard to the chronological sequence of inversions involving chromosome segments 2, 3, and 4 are illustrated. For each scenario, the number of inversions that each junction sequence is involved in is indicated in the table below (GIF 41.4 KB).

10142_2008_99_Fig1_ESM.tif (432 kb)
High resolution (TIF 432 KB).
10142_2008_99_Fig2_ESM.gif (74 kb)
Supplemental Fig. 2

Pedigrees of barley mapping parents Amagi Nijo, Haruna Nijo, WI2585, and Galleon. Dotted lines indicate derivation by selection alone. The extent of backcrossing is not shown (GIF 74.3 KB).

10142_2008_99_Fig2_ESM.tif (963 kb)
High resolution (TIF 962 KB).

References

  1. Aguilera A, Gómez-González B (2008) Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 9:204–217PubMedCrossRefGoogle Scholar
  2. Bilgic H, Cho S, Garvin DF, Muehlbauer GJ (2007) Mapping barley genes to chromosome arms by transcript profiling of wheat–barley ditelosomic chromosome addition lines. Genome 50:898–906PubMedCrossRefGoogle Scholar
  3. Borevitz JO, Hazen SP, Michael TP, Morris GP, Baxter IR, Hu TT, Chen H, Werner JD, Nordborg M, Salf DE, Kay SA, Chory J, Weigel D, Jones JDG, Ecker JR (2007) Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana. Proc Natl Acad Sci U S A 104:12057–12062PubMedCrossRefGoogle Scholar
  4. Bossolini E, Wicker T, Knobel PA, Keller B (2007) Comparison of orthologous loci from small grass genomes Brachypodium and rice: implications for wheat genomics and grass genome annotation. Plant J 49:704–717PubMedCrossRefGoogle Scholar
  5. Brunner S, Keller B, Feuillet C (2003) A large rearrangement involving genes and low-copy DNA interrupts the microcolinearity between rice and barley at the Rph7 locus. Genetics 164:673–683PubMedGoogle Scholar
  6. Bryan GJ, Stephenson P, Collins A, Kirby J, Smith JB, Gale MD (1999) Low levels of DNA sequence variation among adapted genotypes of hexaploid wheat. Theor Appl Genet 99:192–198CrossRefGoogle Scholar
  7. Cáceres M, Ranz JM, Barbadilla A, Long M, Ruiz A (1999) Generation of a widespread Drosophila inversion by a transposable element. Science 285:415–418PubMedCrossRefGoogle Scholar
  8. Caldwell KS, Langridge P, Powell W (2004) Comparative sequence analysis of the region harboring the hardness locus in barley and its colinear region in rice. Plant Physiol 136:3177–3190PubMedCrossRefGoogle Scholar
  9. Carlton JM, Angiuoli SV, Suh BB, Kooij TW, Pertea M, Silva JC, Ermolaeva MD, Allen JE, Selengut JD, Koo HL, Peterson JD, Pop M, Kosack DS, Shumway MF, Bidwell SL, Shallom SJ, van Aken SE, Riedmuller SB, Feldblyum TV, Cho JK, Quackenbush J, Sedegah M, Shoaibi A, Cummings LM, Florens L, Yates JR, Raine JD, Sinden RE, Harris MA, Cunningham DA, Preiser PR, Bergman LW, Vaidya AB, Van Lin LH, Janse CJ, Waters AP, Smith HO, White OR, Salzberg SL, Venter JC, Fraser CM, Hoffman SL, Gardner MJ, Carucci DJ (2002) Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii. Nature 419:512–519PubMedCrossRefGoogle Scholar
  10. Chiapparino E, Lee D, Donini P (2004) Genotyping single nucleotide polymorphisms in barley by tetra-primer ARMS-PCR. Genome 47:414–420PubMedCrossRefGoogle Scholar
  11. Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP (2008) An ALTM1 gene cluster controlling aluminium (aluminum) tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179:669–682PubMedCrossRefGoogle Scholar
  12. Conley EJ, Nduati V, Gonzalez-Hernandez JL, Mesfin A, Trudeau-Spanjers M, Chao S, Lazo GR, Hummel DD, Anderson OD, Qi LL, Gill BS, Echalier B, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dyořák J, Peng JH, Lapitan NLV, Pathan MS, Nguyen HT, Ma XF, Miftahudin, Gustafson JP, Greene RA, Sorrells ME, Hossain G, Kalavacharla V, Kianian SF, Sidhu K, Dijbirligi M, Gill KS, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Anderson JA (2004) A 2600-locus chromosome bin map of wheat homoeologous group 2 reveals interstitial gene-rich islands and colinearity with rice. Genetics 168:625–637PubMedCrossRefGoogle Scholar
  13. Costa JM, Corey A, Hayes PM, Jobet C, Kleinhofs A, Kopisch-Obusch A, Kramer SF, Kudrna D, Li M, Riera-Lizarazu O, Sato K, Szucs P, Toojinda T, Vales MI, Wolfe RI (2001) Molecular mapping of the Oregon Wolfe Barleys: a phenotypically polymorphic doubled-haploid population. Theor Appl Genet 103:415–424CrossRefGoogle Scholar
  14. Dehal P, Predki P, Olsen AS, Kobayashi A, Folta P, Lucas S, Land M, Terry A, Zhou CLE, Rash S, Zhang Q, Gordon L, Kim J, Elkin C, Pollard MJ, Richardson P, Rokhsar D, Uberbacher E, Hawkins T, Branscomb E, Stubbs L (2001) Human chromosome 19 and related regions in mouse: conservative and lineage-specific evolution. Science 293:104–111PubMedCrossRefGoogle Scholar
  15. Dilbirligi M, Erayman M, Gill KS (2005) Analysis of recombination and gene distribution in the 2L1.0 region of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.). Genomics 86:47–54PubMedCrossRefGoogle Scholar
  16. Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan LL, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol 125:1342–1353PubMedCrossRefGoogle Scholar
  17. Dvořák J, Akhunov ED (2005) Tempos of gene locus deletions and duplications and their relationship to recombination rate during diploid and polyploid evolution in the AegilopsTriticum alliance. Genetics 171:323–332PubMedCrossRefGoogle Scholar
  18. Dvořák J, Luo MC, Yang ZL (1998) Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148:423–434PubMedGoogle Scholar
  19. Erayman M, Sandhu D, Sidhu D, Dilbirligi M, Baenziger PS, Gill KS (2004) Demarcating the gene-rich regions of the wheat genome. Nucleic Acids Res 32:3546–3565PubMedCrossRefGoogle Scholar
  20. Franckowiak JD (1996) Revised linkage maps for morphological markers in barley, Hordeum vulgare. Barley Genet Newsl 26:9–21Google Scholar
  21. Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci U S A 95:1971–1974PubMedCrossRefGoogle Scholar
  22. Gaut BS, Wright SI, Rizzon C, Dvořák J, Anderson LK (2007) Opinion—recombination: an underappreciated factor in the evolution of plant genomes. Nat Rev Genet 8:77–84PubMedCrossRefGoogle Scholar
  23. Gottwald S, Stein N, Börner A, Sasaki T, Graner A (2004) The gibberellic-acid insensitive dwarfing gene sdw3 of barley is located on chromosome 2HS in a region that shows high colinearity with rice chromosome 7L. Mol Genet Genomics 271:426–436PubMedCrossRefGoogle Scholar
  24. Hackauf B, Wehling P (2005) Approaching the self-incompatibility locus Z in rye (Secale cereale L.) via comparative genetics. Theor Appl Genet 110:832–845PubMedCrossRefGoogle Scholar
  25. Hori K, Sato K, Nankaku N, Takeda K (2005) QTL analysis in recombinant chromosome substitution lines and doubled haploid lines derived from a cross between Hordeum vulgare ssp. vulgare and Hordeum vulgare ssp. spontaneum. Mol Breed 16:295–311CrossRefGoogle Scholar
  26. Hossain MA, Sparrow DHB (1991) Resistance to powdery mildew (Erysiphe graminis f.sp. hordei) in the barley cultivar Galleon. I. Relationship with known genes for resistance. Euphytica 52:1–9Google Scholar
  27. Huang Y, Zhang L (2004) Rapid and sensitive dot-matrix methods for genome analysis. Bioinformatics 20:460–466PubMedCrossRefGoogle Scholar
  28. Huang S, Spielmeyer W, Lagudah ES, James RA, Platten JD, Dennis ES, Munns R (2006) A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol 142:1718–27PubMedCrossRefGoogle Scholar
  29. Hudson RR, Kaplan NL (1995) Deleterious background selection with recombination. Genetics 141:1605–1617PubMedGoogle Scholar
  30. Jafary H, Szabo LJ, Niks RE (2006) Innate nonhost immunity in barley to different heterologous rust fungi is controlled by sets of resistance genes with different and overlapping specificities. Mol Plant Microb Interact 19:1270–1279CrossRefGoogle Scholar
  31. Jafary H, Albertazzi G, Marcel TC, Niks RE (2008) High diversity of genes for nonhost resistance of barley to heterologous rust fungi. Genetics 178:2327–2339PubMedCrossRefGoogle Scholar
  32. Karakousis A, Barr AR, Kretschmer JM, Manning S, Logue SJ, Roumeliotis S, Collins HM, Chalmers KJ, Li CD, Lance RCM, Langridge P (2003) Mapping and QTL analysis of the barley population Galleon × Haruna Nijo. Aust J Agric Res 54:1131–1135CrossRefGoogle Scholar
  33. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423:241–254PubMedCrossRefGoogle Scholar
  34. Komatsuda T, Tanno K (2004) Comparative high resolution map of the six-rowed spike locus 1 (vrs1) in several populations of barley, Hordeum vulgare L. Hereditas 141:68–73PubMedCrossRefGoogle Scholar
  35. Komatsuda T, Pourkheirandish M, He CF, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, Lundqvist U, Fujimura T, Matsuoka M, Matsumoto T, Yano M (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci U S A 104:1424–1429PubMedCrossRefGoogle Scholar
  36. Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412PubMedGoogle Scholar
  37. Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of 5 major genes and 8 quantitative trait loci controlling flowering time in a winter × spring barley (Hordeum vulgare L.) cross. Genome 38:575–585PubMedGoogle Scholar
  38. Li JZ, Huang XQ, Heinrichs F, Ganal MW, Röder MS (2005) Analysis of QTLs for yield, yield components, and malting quality in a BC3-DH population of spring barley. Theor Appl Genet 110:356–363PubMedCrossRefGoogle Scholar
  39. Marcel TC, Varshney RK, Barbieri M, Jafary H, de Kock MJD, Graner A, Niks RE (2007a) A high-density consensus map of barley to compare the distribution of QTLs for partial resistance to Puccinia hordei and of defence gene homologues. Theor Appl Genet 114:487–500PubMedCrossRefGoogle Scholar
  40. Marcel TC, Aghnoum R, Durand J, Varshney RK, Niks RE (2007b) Dissection of the barley 2L1.0 region carrying the ‘Laevigatum’ quantitiative resistance gene to leaf rust using near-isogenic lines (NIL) and subNIL. Mol Plant Microb Interact 20:1604–1615CrossRefGoogle Scholar
  41. Nduulu LM, Mesfin A, Muehlbauer GJ, Smith KP (2007) Analysis of the chromosome 2(2H) region of barley associated with the correlated traits Fusarium head blight resistance and heading date. Theor Appl Genet 115:561–70PubMedCrossRefGoogle Scholar
  42. Pacher M, Schmidt-Puchta W, Puchta H (2007) Two unlinked double-strand breaks can induce reciprocal exchanges in plant genomes via homologous recombination and nonhomologous end joining. Genetics 175:21–29PubMedCrossRefGoogle Scholar
  43. Pallotta MA, Asayama S, Reinheimer JM, Davies PA, Barr AR, Jefferies SP, Chalmers KJ, Lewis J, Collins HM, Roumeliotis S, Logue SJ, Coventry SJ, Lance RCM, Karakousis A, Lim P, Verbyla AP, Eckermann PJ (2003a) Mapping and QTL analysis of the barley population Amagi Nijo × WI2585. Aust J Agric Res 54:1141–1144CrossRefGoogle Scholar
  44. Pallotta MA, Warner P, Fox RL, Kuchel H, Jeffries SP, Langridge P (2003b) Marker assisted wheat breeding in the southern region of Australia. In: Pogna NE, Romano M, Pogna EA, Galterio G (eds) Proceedings of the 10th international wheat genetics symposium, Paestum, Italy. Istituto Sperimentale per la Cerealicoltura, Roma, pp 789–791Google Scholar
  45. Perovic D, Stein N, Zhang H, Drescher A, Prasad M, Kota R, Kopahnke D, Graner A (2004) An integrated approach for comparative mapping in rice and barley with special reference to the Rph16 resistance locus. Funct Integr Genomics 4:74–83PubMedCrossRefGoogle Scholar
  46. Pevzner P, Tesler G (2003) Human and mouse genomic sequences reveal extensive breakpoint reuse in mammalian evolution. Proc Natl Acad Sci U S A 100:7672–7677PubMedCrossRefGoogle Scholar
  47. Pillen K, Zacharias A, Léon J (2003) Advanced backcross QTL analysis in barley (Hordeum vulgare L.). Theor Appl Genet 107:340–352PubMedCrossRefGoogle Scholar
  48. Pillen K, Zacharias A, Léon J (2004) Comparative AB-QTL analysis in barley using a single exotic donor of Hordeum vulgare ssp. spontaneum. Theor Appl Genet 108:1591–1601PubMedCrossRefGoogle Scholar
  49. Pourkheirandish M, Wicker T, Stein N, Fujimura T, Komatsuda T (2007) Analysis of the barley chromosome 2 region containing the six-rowed spike gene vrs1 reveals a breakdown of rice-barley micro colinearity by a transposition. Theor Appl Genet 114:1357–65PubMedCrossRefGoogle Scholar
  50. Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvořák J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma XF, Miftahudin, Gustafson JP, Conley EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712PubMedCrossRefGoogle Scholar
  51. Ramakrishna W, Dubcovsky J, Park YJ, Busso C, Emberton J, SanMiguel P, Bennetzen JL (2002) Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. Genetics 162:1389–1400PubMedGoogle Scholar
  52. Rattray AJ, Strathern JN (2003) Error-prone DNA polymerases: when making a mistake is the only way to get ahead. Annu Rev Genet 37:31–66PubMedCrossRefGoogle Scholar
  53. Reinheimer JL, Barr AR, Eglinton JK (2004) QTL mapping of chromosomal regions conferring reproductive frost tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 109:1267–1274PubMedCrossRefGoogle Scholar
  54. Rogowsky PM, Guidet FLY, Langridge P, Shepherd KW, Koebner RMD (1991) Isolation and characterization of wheat–rye recombinants involving chromosome arm 1DS of wheat. Theor Appl Genet 82:537–544CrossRefGoogle Scholar
  55. 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
  56. Shin JS, Chao S, Corpuz L, Blake T (1990) A partial map of the barley genome incorporating restriction fragment length polymorphism, polymerase chain reaction, isozyme, and morphological marker loci. Genome 33:803–810PubMedGoogle Scholar
  57. Sidhu D, Gill KS (2004) Distribution of genes and recombination in wheat and other eukaryotes. Plant Cell Tiss Org 79:257–270CrossRefGoogle Scholar
  58. Sorrells ME, La Rota M, Bermudez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Miftahudin, Mahmoud A, Ma XF, Gustafson PJ, Qi LLL, Echalier B, Gill BS, Matthews DE, Lazo GR, Chao SM, Anderson OD, Edwards H, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvořák J, Zhang DS, Nguyen HT, Peng JH, Lapitan NLV, Gonzalez-Hernandez JL, Anderson JA, Hossain K, Kalavacharla V, Kianian SF, Choi DW, Close TJ, Dilbirligi M, Gill KS, Steber C, Walker-Simmons MK, McGuire PE, Qualset CO (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827PubMedGoogle Scholar
  59. Stankiewicz P, Lupski JR (2002) Genome architecture, rearrangements and genomic disorders. Trends Genet 18:74–82PubMedCrossRefGoogle Scholar
  60. Stein N, Prasad M, Scholz U, Thiel T, Zhang HN, Wolf M, Kota R, Varshney RK, Perovic D, Grosse I, Graner A (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114:823–839PubMedCrossRefGoogle Scholar
  61. Sutton T, Baumann U, Hayes J, Collins NC, Shi BJ, Schnurbusch T, Hay A, Mayo G, Pallotta M, Tester M, Langridge P (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–1449PubMedCrossRefGoogle Scholar
  62. Tabone T, Hayden M (2007) Method of amplifying nucleic acid. USPTO, USAGoogle Scholar
  63. 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
  64. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034PubMedCrossRefGoogle Scholar
  65. Turuspekov Y, Mano Y, Honda I, Kawada N, Watanabe Y, Komatsuda T (2004) Identification and mapping of cleistogamy genes in barley. Theor Appl Genet 109:480–487PubMedCrossRefGoogle Scholar
  66. Turuspekov Y, Kawada N, Honda I, Watanabe Y, Komatsuda T (2005) Identification and mapping of a QTL for rachis internode length associated with cleistogamy in barley. Plant Breed. 124:542–545CrossRefGoogle Scholar
  67. Valárik M, Linkiewicz A, Dubcovsky J (2006) A microcolinearity study at the earliness per se gene Eps-A m 1 region reveals an ancient duplication that preceded the wheat–rice divergence. Theor Appl Genet 112:945–957PubMedCrossRefGoogle Scholar
  68. von Korff M, Wang H, Léon J, Pillen K (2006) AB-QTL analysis in spring barley: II. Detection of favourable exotic alleles for agronomic traits introgressed from wild barley (H. vulgare ssp. spontaneum). Theor Appl Genet 112:1221–31CrossRefGoogle Scholar
  69. Ziolkowski PA, Blanc G, Sadowski J (2003) Structural divergence of chromosomal segments that arose from successive duplication events in the Arabidopsis genome. Nucleic Acids Res 31:1339–1350PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Andrew Chen
    • 1
  • Anita Brûlé-Babel
    • 2
  • Ute Baumann
    • 1
  • Nicholas C. Collins
    • 1
  1. 1.Australian Centre for Plant Functional Genomics (ACPFG), School of Agriculture, Food and WineUniversity of AdelaideGlen OsmondAustralia
  2. 2.Department of Plant ScienceUniversity of ManitobaWinnipegCanada

Personalised recommendations