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Analysis of the barley chromosome 2 region containing the six-rowed spike gene vrs1 reveals a breakdown of rice–barley micro collinearity by a transposition

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Abstract

In cultivated barley (Hordeum vulgare ssp. vulgare), six-rowed spikes produce three times as many seeds per spike as do two-rowed spikes. The determinant of this trait is the Mendelian gene vrs1, located on chromosome 2H, which is syntenous with rice (Oryza sativa) chromosomes 4 and 7. We exploited barley–rice micro-synteny to increase marker density in the vrs1 region as a prelude to its map-based cloning. The rice genomic sequence, covering a 980 kb contig, identified barley ESTs linked to vrs1. A high level of conservation of gene sequence was obtained between barley chromosome 2H and rice chromosome 4. A total of 22 EST-based STS markers were placed within the target region, and the linear order of these markers in barley and rice was identical. The genetic window containing vrs1 was narrowed from 0.5 to 0.06 cM, which facilitated covering the vrs1 region by a 518 kb barley BAC contig. An analysis of the contig sequence revealed that a rice Vrs1 orthologue is present on chromosome 7, suggesting a transposition of the chromosomal segment containing Vrs1 within barley chromosome 2H. The breakdown of micro-collinearity illustrates the limitations of synteny cloning, and stresses the importance of implementing genomic studies directly in the target species.

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References

  • Akhunov ED, Goodyear AW, Geng S, Qi L-L, Echalier B, Gill BS, Miftahudin, Gustafson JP, Lazo G, Chao S, Anderson OD, Linkiewicz AM, Dubcovsky J, La Rota M, Sorrells ME, Zhang D, Nguyen HT, Kalavacharla V, Hossain K, Kianian SF, Peng J, Lapitan NLV, Gonzalez-Hernandez JL, Anderson JA, Choi D-W, Close TJ, Dilbirligi M, Gill KS, Walker-Simmons MK, Steber C, McGuire PE, Qualset CO, Dvorak J (2003) The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. Genome Res 13:753–763

    Article  PubMed  CAS  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218

    CAS  Google Scholar 

  • Bennetzen JL, Ma J (2003) The genetic colinearity of rice and other cereals on the basis of genomic sequence analysis. Curr Opin Plant Biol 6:128–133

    Article  PubMed  CAS  Google Scholar 

  • Bothmer Rv, Jacobsen N (1985) Origin, taxonomy, and related species. In: Rasmusson D (ed) Barley-ASA agronomy monograph, vol 26. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, WI, pp 19–56

  • Bothmer Rv, Jacobsen N, Baden C, Jørgensen RB, Linde-Laursen I (1995) An ecogeographical study of the genus Hordeum, 2nd edn. Systematic and ecogeographic studies on crop genepools 7. International Plant Genetic Resources Institute, Rome

  • Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA 99:9328–9333

    Article  PubMed  CAS  Google Scholar 

  • Brunner S, Keller B, Feuillet C (2003) A large rearrangement involving genes and low-copy DNA interrupts the microcollinearity between rice and barley at the Rph7 locus. Genetics 164:673–683

    PubMed  CAS  Google Scholar 

  • 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 136:3177–3190

    Article  PubMed  CAS  Google Scholar 

  • Chantret N, Cenci A, Sabot F, Anderson O, Dubcovsky J (2004) Sequencing of the Triticum monococcum hardness locus reveals good microcolinearity with rice. Mol Gen Genomics 271:377–386

    Article  CAS  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977

    Article  PubMed  CAS  Google Scholar 

  • Devos KM (2005) Updating the ‘Crop Circle’. Curr Opin Plant Biol 8:155–162

    Article  PubMed  CAS  Google Scholar 

  • Doust AN, Devos KM, Gadberry MD, Gale MD, Kellogg EA (2004) Genetic control of branching in foxtail millet. Proc Natl Acad Sci USA 101:9045–9050

    Article  PubMed  CAS  Google Scholar 

  • Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol 125:1342–1353

    Article  PubMed  CAS  Google Scholar 

  • Dunford RP, Yano M, Kurata N, Sasaki T, Huestis G, Rocheford T, Laurie DA (2002) Comparative mapping of the barley Ppd-H1 photoperiod response gene region, which lies close to a junction between two rice linkage segments. Genetics 161:825–834

    PubMed  CAS  Google Scholar 

  • Feuillet C, Keller B (1999) High gene density is conserved at syntenic loci of small and large grass genomes. Proc Natl Acad Sci USA 96:8265–8270

    Article  PubMed  CAS  Google Scholar 

  • Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974

    Article  PubMed  CAS  Google Scholar 

  • Gill KS, Gill BS, Endo TR, Boyko EV (1996) Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics 143:1001–1012

    PubMed  CAS  Google Scholar 

  • 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 Gen Genomics 271:426–436

    Article  CAS  Google Scholar 

  • Griffee F (1925) Correlated inheritance of botanical characters in barley, and manner of reaction to Helminthosporium sativum. J Agric Res 30:915–935

    Google Scholar 

  • Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, Reader S, Colas I, Moore G (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439:749–752

    Article  PubMed  CAS  Google Scholar 

  • Harlan JR (1995) Barley. In: Smartt J, Simmonds NW (eds) Evolution of crop plants, 2nd edn. Longman, New York, pp 140–147

    Google Scholar 

  • He C, Sayed-Tabatabaei BE, Komatsuda T (2004) AFLP targeting of the 1-cM region conferring the vrs1 gene for six-rowed spike in barley, Hordeum vulgare L. Genome 47:1122–1129

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (IRGSP) (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Kleinhofs A, Kilian A, Saghai Maroof MA, Biyashev RM, Hayes P, Chen FQ, Lapitan N, Fenwick A, Blake TK, Kanazin V, Ananiev E, Dahleen L, Kudrna D, Bollinger J, Knapp SJ, Liu B, Sorrells M, Heun M, Franckowiak JD, Hoffman D, Skadsen R, Steffenson BJ (1993) A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome. Theor Appl Genet 86:705–712

    Article  CAS  Google Scholar 

  • Komatsuda T, Nakamura I, Takaiwa F, Oka S (1998) Development of STS markers closely linked to the vrs1 locus in barley, Hordeum vulgare. Genome 41:680–685

    Article  CAS  Google Scholar 

  • Komatsuda T, Pourkheirandish M, He C, 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 USA 104:1424–1429

    Google Scholar 

  • 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 141:68–73

    Article  PubMed  CAS  Google Scholar 

  • Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412

    PubMed  Google Scholar 

  • Laurie DA (1997) Comparative genetics of flowering time. Plant Mol Biol 35:167–177

    Article  PubMed  CAS  Google Scholar 

  • Li W, Gill BS (2002) The colinearity of the Sh2/A1 orthologous region in rice, sorghum and maize is interrupted and accompanied by genome expansion in the Triticeae. Genetics 160:1153–1162

    PubMed  CAS  Google Scholar 

  • Lichten M, Goldman ASH (1995) Meiotic recombination hotspots. Annu Rev Genet 29:423–444

    Article  PubMed  CAS  Google Scholar 

  • Makino T, Furusho M, Fukuoka T (1995) A mutant having six-rowed gene allelic to v locus. Barley Genet Newsl 24:122

    Google Scholar 

  • Moore G (1995) Cereal genome evolution: pastoral pursuits with ‘Lego’ genomes. Curr Opin Genet Dev 5:717–724

    Article  PubMed  CAS  Google Scholar 

  • 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 4:74–83

    Article  PubMed  CAS  Google Scholar 

  • Ramakrishna W, Dubcovsky J, Park Y-J, 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 162:1389–1400

    PubMed  CAS  Google Scholar 

  • Robertson DW, Wiebe GA, Shands RG, Hagberg A (1965) A summary of linkage studies in cultivated barley, Hordeum species: supplement III, 1954–1963. Crop Sci 5:33–43

    Article  Google Scholar 

  • Rostoks N, Mudie S, Cardle L, Russell J, Ramsay L, Booth A, Svensson JT, Wanamaker SI, Walia H, Rodriguez EM, Hedley PE, Liu H, Morris J, Close TJ, Marshall DF, Waugh R (2005) Genome-wide SNP discovery and linkage analysis in barley based on genes responsive to abiotic stress. Mol Gen Genomics 274:515–527

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • SanMiguel P, Tikhonov A, Jin Y-K, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768

    Article  PubMed  CAS  Google Scholar 

  • Schnable PS, Hsia A-P, Nikolau BJ (1998) Genetic recombination in plants. Curr Opin Plant Biol 1:123–129

    Article  PubMed  CAS  Google Scholar 

  • Shepherd K, Islam AKMR (1981) Wheat: barley hybrids-the first eighty years. In: Evans RT, Peacock KW (eds) Wheat science today and tomorrow. Cambridge University Press, Cambridge, New York, pp 107–128

    Google Scholar 

  • Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S, Ordon F, Graner A (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42:912–922

    Article  PubMed  CAS  Google Scholar 

  • Tarchini R, Biddle P, Wineland R, Tingey S, Rafalski A (2000) The complete sequence of 340 kb of DNA around the rice Adh1–Adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell 12:381–391

    Article  PubMed  CAS  Google Scholar 

  • Tikhonov AP, SanMiguel PJ, Nakajima Y, Gorenstein NM, Bennetzen JL, Avramova Z (1999) Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96:7409–7414

    Article  PubMed  CAS  Google Scholar 

  • Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034

    Article  PubMed  CAS  Google Scholar 

  • Wei F, Gobelman-Werner K, Morroll SM, Kurth J, Mao L, Wing R, Leister D, Schulze-Lefert P, Wise RP (1999) The Mla (Powdery Mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. Genetics 153:1929–1948

    PubMed  CAS  Google Scholar 

  • Wicker T, Stein N, Albar L, Feuillet C, Schlagenhauf E, Keller B (2001) Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J 26:307–316

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Tomkins JP, Waugh R, Frisch DA, Kudrna D, Kleinhofs A, Brueggeman RS, Muehlbauer GJ, Wise RP, Wing RA (2000) A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor Appl Genet 101:1093–1099

    Article  CAS  Google Scholar 

  • Zohary D (1963) Spontaneous brittle six-rowed barley, their nature and origin. Barley Genetics I. In: Proceedings of the 1st International Barley Genet Symposium, Wageningen 1963, Pudoc, Wageningen, The Netherlands, pp 27–31

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Acknowledgements

We thank M. Sameri, S. Okamura, M. Chono, J. Song and Y. Nagamura for their help and advice. We also thank M. Matsuoka, Y. Turuspekov and P. Azhaguvel for useful discussions. We thank R. Koebner for linguistic assistance in the preparation of this manuscript. The financial support of the Ministry of Agriculture, Forestry and Fisheries of Japan is acknowledged (Rice Genome Project MP1113b and Green Techno Project GD3006). M. Pourkheirandish was a research fellow supported by Japan International Research Center for Agricultural Sciences (JIRCAS).

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Authors and Affiliations

  1. National Institute of Agrobiological Sciences (NIAS), Tsukuba, 305-8602, Japan

    M. Pourkheirandish & T. Komatsuda

  2. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 305-8572, Japan

    M. Pourkheirandish & T. Fujimura

  3. Institute of Plant Biology, University of Zürich, Zürich, 8008, Switzerland

    T. Wicker

  4. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, 06466, Germany

    N. Stein

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  1. M. Pourkheirandish
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  2. T. Wicker
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Correspondence to T. Komatsuda.

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Communicated by B. Keller.

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Pourkheirandish, M., Wicker, T., Stein, N. et al. Analysis of the barley chromosome 2 region containing the six-rowed spike gene vrs1 reveals a breakdown of rice–barley micro collinearity by a transposition. Theor Appl Genet 114, 1357–1365 (2007). https://doi.org/10.1007/s00122-007-0522-4

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