Skip to main content
Log in

A high-density cytogenetic map of the Aegilops tauschii genome incorporating retrotransposons and defense-related genes: insights into cereal chromosome structure and function

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Aegilops tauschii (Coss.) Schmal. (2n=2x=14, DD) (syn. A. squarrosa L.; Triticum tauschii) is well known as the D-genome donor of bread wheat (T. aestivum, 2n=6x=42, AABBDD). Because of conserved synteny, a high-density map of the A. tauschii genome will be useful for breeding and genetics within the tribe Triticeae which besides bread wheat also includes barley and rye. We have placed 249 new loci onto a high-density integrated cytological and genetic map of A. tauschii for a total of 732 loci making it one of the most extensive maps produced to date for the Triticeae species. Of the mapped loci, 160 are defense-related genes. The retrotransposon marker system recently developed for cultivated barley (Hordeum vulgare L.) was successfully applied to A. tauschii with the placement of 80 retrotransposon loci onto the map. A total of 50 microsatellite and ISSR loci were also added. Most of the retrotransposon loci, resistance (R), and defense-response (DR) genes are organized into clusters: retrotransposon clusters in the pericentromeric regions, R and DR gene clusters in distal/telomeric regions. Markers are non-randomly distributed with low density in the pericentromeric regions and marker clusters in the distal regions. A significant correlation between the physical density of markers (number of markers mapped to the chromosome segment/physical length of the same segment in μm) and recombination rate (genetic length of a chromosome segment/physical length of the same segment in μm) was demonstrated. Discrete regions of negative or positive interference (an excess or deficiency of crossovers in adjacent intervals relative to the expected rates on the assumption of no interference) was observed in most of the chromosomes. Surprisingly, pericentromeric regions showed negative interference. Islands with negative, positive and/or no interference were present in interstitial and distal regions. Most of the positive interference was restricted to the long arms. The model of chromosome structure and function in cereals with large genomes that emerges from these studies is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.

    Google Scholar 

  • Arumuganathan, K. and Earle, E.D. 1991. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9: 208-218.

    Google Scholar 

  • Bennett, M.D. and Leitch, I.J. 1995. Nuclear DNA amounts in Angiosperms. Ann. Bot. 76: 113-176.

    Google Scholar 

  • Boyko, E.V., Gill, K.S., Mickelson-Young, L., Nasuda, S., Raupp, W.J., Ziegle, J.N., Singh, S., Hassawi, D.S., Fritz, A.K., Namuth, D., Lapitan, N.L.V. and Gill, B.S. 1999. A high-density genetic linkage map of Aegilops tauschii, the D-genome progenitor of bread wheat. Theor. Appl. Genet. 99: 16-26.

    Google Scholar 

  • Bryngelsson, T., Sommer-Knudsen, J., Gregersen, P.L., Collinge, D.B., Ek, B. and Thordal-Christensen, H. 1994. Purification, characterization, and molecular cloning of basic PR-1-type pathogenesis-related proteins from barley. Mol. Plant-Microbe Interact. 7: 267-275.

    Google Scholar 

  • Caron, H., van Schaik, B., van der Mee, M., Baas, F., Riggins, G., van Sluis, P., Hermus, M.-C., van Asperen, R., Boon, K., Voute, P.A., Heisterkamp, S., van Kampen, A. and Versteeg, R. 2001. The human transcriptome map: clustering of highly expressed genes in chromosomal domains. Science 291: 1289-1292.

    Google Scholar 

  • Collins, N.C., Webb, C.A., Seah, S., Ellis, J.G., Hulbert, S.H. and Pryor, A. 1998. The isolation and mapping of disease resistance gene analogs in maize. Mol. Plant-Microbe Interact. 11: 968-978.

    Google Scholar 

  • Creusot, F., Macadré, C., Ferrier Cana, E., Riou, C., Geffroy, V., Sévignac, M., Dron, M. and Langin, T. 1999. Cloning and molecular characterization of three members of the NBS-LRR subfamily located in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris. Genome 42: 254-264.

    Google Scholar 

  • Delaney, D.E., Nasuda, S., Endo, T.R., Gill, B.S. and Hulbert, S.H. 1995a. Cytologically based physical maps of the group-2 chromosomes of wheat. Theor. Appl. Genet. 91: 568-573.

    Google Scholar 

  • Delaney, D.E., Nasuda, S., Endo, T.R., Gill, B.S. and Hulbert, S.H. 1995b. Cytologically based physical maps of the group-3 chromosomes of wheat. Theor. Appl. Genet. 91: 780-782.

    Google Scholar 

  • Denell, R.E. and Keppy, D.O. 1979. The nature of genetic recombination near the third chromosome centromere of Drosophila melanogaster. Genetics 93: 117-130.

    Google Scholar 

  • Dvorák, J., Luo, M.-C., Yang, Z.-L. 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: 423-434.

    Google Scholar 

  • Egel-Mitani, M., Olsson, L.W. and Egel, R. 1982. Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas 97: 179-187.

    Google Scholar 

  • Ellis, J.G., Lawrence, G.J., Luck, J.E. and Dodds, P.N. 1999. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11: 495-506.

    Google Scholar 

  • Endo, T.R. and Gill, B.S. 1996. The deletion stocks of common wheat. J. Hered. 87: 295-307.

    Google Scholar 

  • European Union Chromosome 3 Arabidopsis Sequencing Consortium and Institute for Genomic Research and Kazusa DNA Research Institute. 2000. Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana. Nature 408: 820-822.

    Google Scholar 

  • Ewing, B. and Green, P. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8: 186-194.

    Google Scholar 

  • Ewing, B., Hillier, L., Wendl, M.C., and Green, P. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175-185.

    Google Scholar 

  • Faris, J.D., Li, W.L., Liu, D.J., Chen, P.D. and Gill, B.S. 1999. Candidate gene analysis of quantitative disease resistance in wheat. Theor. Appl. Genet. 98: 219-225.

    Google Scholar 

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

    Google Scholar 

  • Flavell, A.J., Knox, M.R., Pearce, S.R. and Ellis, T.H.N. 1998. Retrotransposon-based insertion polymorphisms (RBIP) for high through-put marker analysis. Plant J. 16: 643-650.

    Google Scholar 

  • Friebe, Mukai Y. ans Gill B.S. 1992. C-banding polymorphism in several accessions of Triticum tauschii. Genome 35: 192-199.

    Google Scholar 

  • Geffroy, V., Sicard, D., de Olivera, J.C.F., Sévignac, M., Cohen, S., Gepts, P., Neema, C., Langin, T. and Dron, M. 1999. Identification of an ancestral resistance gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum. Mol. Plant-Microbe Interact. 12: 774-784.

    Google Scholar 

  • Gill, B.S., Friebe, B. and Endo, T.R. 1991a. Stardard karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome 34: 830-839.

    Google Scholar 

  • Gill, K.S., Lubbers, E.L., Gill, B.S., Raupp, W.J. and Cox, T.S. 1991b. A genetic linkage map of Triticum tauschii (DD) and its relationship to the D genome of bread wheat (AABBDD). Genome 34: 362-374.

    Google Scholar 

  • Gill, K.S., Gill, B.S. and Endo, T.R. 1993. A chromosome region-specific mapping strategy reveals gene-rich telomeric ends in wheat. Chromosoma 102: 374-381.

    Google Scholar 

  • Gill, K.S., Gill, B.S., Endo, T.R. and Boyko, E.V. 1996a. Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics 143: 1001-1012.

    Google Scholar 

  • Gill, K.S., Gill, B.S., Endo, T.R. and Taylor, T. 1996b. Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics 144: 1883-1891.

    Google Scholar 

  • Gordon, D., Abajian, C., and Green, P. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8: 195-202.

    Google Scholar 

  • Green, M.M. 1975. Conversion as a possible mechanism of high coincidence values in the centromere region of Drosophila. Mol. Gen. Genet. 139: 57-66.

    Google Scholar 

  • Gribbon, B.M., Pearce, S.R., Kalendar, R., Schulman, A.H., Jack, P., Kumar, A. and Flavell, A.J. 1999. Phylogeny and transpositional activity of Ty1-copia group retrotransposons in cereal genomes. Mol. Gen. Genet. 261: 883-891.

    Google Scholar 

  • Hohmannn, U., Endo, T.R., Gill, K.S. and Gill, B.S. 1994. Comparison of genetic and physical maps of group-7 chromosomes from Triticum aestivum L. Mol. Gen. Genet. 245: 644-653.

    Google Scholar 

  • International Human Genome Sequencing Consortium 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-920.

    Google Scholar 

  • Jääskeläinen, M., Mykkänen, A-H., Arna, T., Vicient, C., Suoniemi, A., Kalendar, R., Savilahti, H. and Schulman, A.H. 1999. Retrotransposon BARE-1: expression of encoded proteins and formation of virus-like particles in barley cells. Plant J. 20: 413-422.

    Google Scholar 

  • Kalendar, R., Grob, T., Regina, M., Suoniemi, A. and Schulman, A.H. 1999. IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor. Appl. Genet. 98: 704-711.

    Google Scholar 

  • Kalendar, R., Tanskanen, J., Immonen, S., Nevo, E. and Schulman, A.H. 2000. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc. Natl. Acad. Sci. USA 96: 6603-6607.

    Google Scholar 

  • Kam-Morgan, L.N.W., Gill, B.S. and Muthukrishnan, S. 1989. DNA restriction fragment length polymorphisms: a strategy for genetic mapping of D genome of wheat. Genome 32: 724-732.

    Google Scholar 

  • Kanazin, V., Marek, L.F. and Shoemaker, R.C. 1996. Resistance gene analogs are conserved and clustered in soybean. Proc. Natl. Acad. Sci. USA 93: 11746-11750.

    Google Scholar 

  • Kazusa DNA Research Institute, Cold Spring Harbor Laboratory, Washington University in St. Louis Sequencing Consortium, and European Union Arabidopsis Genome Sequencing Consortium. 2000. Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana. Nature 408: 823-826.

    Google Scholar 

  • Kesseli, R., Witsenboer, H., Stanghellini, M., Vandermark, G. and Michelmore, R. 1993. Recessive resistance to Plasmopara lactucae-radicis maps by bulked segregant analysis to a cluster of dominant disease resistance genes in lettuce. Mol. Plant-Microbe Interact. 6: 722-728.

    Google Scholar 

  • Korol, A.B., Preygel, I.A. and Preygel, S.I. 1994. Recombination Variability and Evolution Algorithms of Estimation and Population Genetics Models. Chapman and Hall, London.

    Google Scholar 

  • Kumar, A. and Bennetzen, J. 1999. Plant retrotransposons. Annu. Rev. Genet. 33: 479-532.

    Google Scholar 

  • Kunzel, G., Korzun, L., and Meister A. 2000. Cytologically integrated physical RFLP maps for the barley genome based on translocation breakpoints. Genetics 154: 397-412.

    Google Scholar 

  • Lake, S. 1986. Recombination frequencies and the coincidence in proximal X-chromosome regions including heterochromatin in Drosophila melanogaster. Hereditas 105: 263-268.

    Google Scholar 

  • Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincoln, S.E. and Newburg, L. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 81-181.

    Google Scholar 

  • Leister, D., Kurth, J., Laurie, D.A., Yano, M., Sasaki, T., Devos, K., Graner, A. and Schulze-Lefert, P. 1998. Rapid reorganization of resistance gene homologues in cereal genomes. Proc. Natl. Acad. Sci. USA 95: 370-375.

    Google Scholar 

  • Leister, D., Kurth, J., Laurie, D.A., Yano, M., Sasaki, T., Graner, A. and Schulze-Lefert, P. 1999. RFLP and physical mapping of resistance gene homologues in rice (O. sativa) and barley (H. vulgare). Theor. Appl. Genet. 98: 509-520.

    Google Scholar 

  • Li, H. and Gill, B.S. 2001. An RGA-like marker detects all known Lr21 leaf rust resistance gene family members in Aegilops tauschii and wheat. Theor. Appl. Genet., in press.

  • Li, W.L., Faris, J.D., Chittoor, J.M., Leach, J.E., Hulbert, S.H., Liu, D.J., Chen, P.D. and Gill, B.S. 1999. Genomic mapping of defense response genes in wheat. Theor. Appl. Genet. 98: 226-233.

    Google Scholar 

  • Manninen, O., Kalendar, R., Robinson, J. and Schulman, A.H. 2000. Application of BARE-1 retrotransposon markers to map a major resistance gene for net blotch in barley. Mol. Gen. Genet. 264: 325-334.

    Google Scholar 

  • Matsuoka, Y. and Tsunewaki K. 1996. Wheat retrotransposon families identified by reverse transcriptase domain analysis. Mol. Biol. Evol. 13: 1384-1392.

    Google Scholar 

  • McClave, J.T. and Dietrich, F.H. II. 1982. Statistics. Dellen Publishing Company, San Francisco/Santa Clara, CA, 766 pp.

    Google Scholar 

  • Mickelson-Young, L., Endo, T.R. and Gill, B.S. 1995. A cytogenetic ladder-map of the wheat homoeologous group-4 chromosomes. Theor. Appl. Genet. 90: 1007-1011.

    Google Scholar 

  • Muthukrishnan, S., Liang, G.H., Trick, H.N. and Gill B.S. 2001. Pathogenesis-related proteins and their genes in cereals. Plant Cell Tissue Organ Cult. 64: 93-114.

    Google Scholar 

  • Noël, L., Moores, T.L., van der Biezen, E.A., Parniske, M., Daniels, M.J., Parker, J.E. and Jones, J.D.G. 1999. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11: 2099-2111.

    Google Scholar 

  • Panstruga, R., Büschges, R., Piffanelli, P. and Schulze-Lefert, P. 1998. A contiguous 60 kb genomic stretch from barley reveals molecular evidence for gene islands in a monocot genome. Nucl. Acids Res. 26: 1056-1062.

    Google Scholar 

  • Pearce, S.R., Harrison, G., Heslop-Harrison, J.S., Flavell, A.J. and Kumar, A. 1997. Characterization and genomic organization of Ty1-copia group retrotransposons in rye (Secale cereale). Genome 40: 1-9.

    Google Scholar 

  • Pearce, S.R., Stuart-Rogers, C., Knox, M.R., Kumar, A., Noel-Ellis, T.H. and Flavell, A.J. 1999. Rapid isolation of plant Ty1-copia group retrotransposon LTR sequences for molecular marker studies. Plant J. 19: 711-717.

    Google Scholar 

  • Peng, J., Korol, A.B., Fahima, T., Röder, M.S., Ronin, Y.I., Li, Y.C. and Nevo, E. 2000. Molecular genetic maps of wild emmer wheat, Triticum diccocoides: genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Res. 10: 1509-1531.

    Google Scholar 

  • Plaschke, J., Börner, A., Wendehake, K., Ganal, M.W. and Röder, M.S. 1996. The use of wheat aneuploids for the chromosomal assignment of microsatellite loci. Euphytica 89: 33-40.

    Google Scholar 

  • Ramsay, L., Macaulay, M., Carle, L., Morgante, M., Degli-Ivanissevich, S., Maestri, E., Powell, W. and Waugh, R. 1999. Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant J. 17: 415-425.

    Google Scholar 

  • Raupp, W.J., Singh, S., Brown-Guedira, G.L. and Gill, B.S. 2001. Cytogenetic and molecular mapping of the leaf rust resistance gene Lr39 in wheat. Theor. Appl. Genet. 102: 347-352.

    Google Scholar 

  • Rivkin, M.I., Vallejos, C.E. and McClean, P.E. 1999. Disease-resistance related sequences in common bean. Genome 42: 41-47.

    Google Scholar 

  • Röder, M.S., Plaschke, J., König, S.U., Börner, A., Sorrells, M.E., Tanksley, S.D. and Ganal, M.W. 1995. Abundance, variability and chromosomal location of microsatellites in wheat. Mol. Gen. Genet. 246: 327-333.

    Google Scholar 

  • Röder, M.S., Korzun, V., Wendehake, K., Plaschke, J., Tixier, M-H., Leroy, P. and Ganal, M.W. 1998. A microsatellite map of the wheat genome. Genetics 149: 2007-2023.

    Google Scholar 

  • Sandhu, D., Champoux, J.A., Bondareva, S.N. and Gill, K.S. 2001. Identification and physical localization of useful genes and markers to a major gene-rich region on wheat group 1S chromosomes. Genetics 157: 1735-1747.

    Google Scholar 

  • Schnable, P.S., Hsia, A.P. and Nikolau, B.J. 1998. Genetic recombination in plants. Curr. Opin. Plant Biol. 1(2): 123-129.

    Google Scholar 

  • Seah, S., Sivasithamparam, K., Karakousis, A. and Lagudah, E.S. 1998. Cloning and characterization of a family of disease resistance gene analogs from wheat and barley. Theor. Appl. Genet. 97: 937-945.

    Google Scholar 

  • Seah, S., Spielmeyer, W., Jahier, J., Sivasithamparam, K. and Lagudah, E.S. 2000. Resistance gene analogs within an introgressed chromosomal segment derived from Triticum ventricosum that confers resistance to nematode and rust pathogens in wheat. Mol. Plant-Microbe Interact. 13: 334-341.

    Google Scholar 

  • Shirasu, K., Schulman, A.H., Lahaye, T. and Schulze-Lefert, P. 2000. A contiguous 66 kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res. 10: 908-915.

    Google Scholar 

  • Sicard, D., Woo, S.-S., Arroyo-Garcia, R., Ochoa, O., Nguyen, D., Korol, A., Nevo, E. and Michelmore, R. 1999. Molecular diversity at the major cluster of disease resistance genes in cultivated and wild Lactuca ssp. Theor. Appl. Genet. 99: 405-418.

    Google Scholar 

  • Sinclair, D.A. 1975. Crossing over between closely linked markers spanning the centromere of chromosome 3 in Drosophila melanogaster. Genet. Res. 11: 173-185.

    Google Scholar 

  • Spielmeyer, W., Robertson, M., Collins, N., Leister, N., Schulze-Lefert, P., Seah, S., Moullet, O. and Lagudah, E.S. 1998. A superfamily of disease resistance gene analogs is located on all homoeologous groups of wheat (Triticum aestivum). Genome 41: 782-788.

    Google Scholar 

  • Spielmeyer, W., Moullet, O., Laroche, A. and Lagudah, E. S. 2000. Highly recombinogenic regions at seed storage protein loci on chromosome 1DS of Aegilops tauschii, the D-genome donor of wheat. Genetics 155: 361-367.

    Google Scholar 

  • Suoniemi, A., Anamthawat-Jónsson, K., Arna, T. and Schulman, A.H. 1996a. Retrotransposon BARE-1 is a major, dispersed component of the barley (Hordeum vulgare L.) genome. Plant Mol. Biol. 30: 1321-1329.

    Google Scholar 

  • Suoniemi, A., Narvanto, A. and Schulman, A. 1996b. The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol. Biol. 31: 295-306.

    Google Scholar 

  • Sybenga, J. 1996. Recombination and chiasmata: few but intriguing discrepancies. Genome 39: 473-484.

    Google Scholar 

  • Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J. et al. 2001. The sequence of the human genome. Science 291: 1304-1351.

    Google Scholar 

  • Vicient, C.M., Suoniemi, A., Anamthawat-Jónsson, K., Tanskanen, J., Beharav, A., Nevo, E. and Schulman, A.H. 1999. Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11: 1769-1784.

    Google Scholar 

  • Vicient, C.M., Jääskeläinen, M., Kalendar, R. and Schulman, A.H. 2001. Active retrotransposons are a common feature of grass genomes. Plant Physiol. 125: 1283-1292.

    Google Scholar 

  • Waugh, R., McLean, K., Flavell, A.J., Pearce, S.R., Kumar, A., Thomas, B.B.T. and Powell, W. 1997. Genetic distribution of BARE-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (SSAP). Mol. Gen. Genet. 253: 687-694.

    Google Scholar 

  • Weng, Y., Tuleen, N.A. and Hart, G.E. 2000. Extended physical maps and consensus physical map of the homoeologous group-6 chromosomes of wheat (Triticum aestivum L. em Thell.). Theor. Appl. Genet. 100: 519-527.

    Google Scholar 

  • WGRC home page: http//www.ksu.edu/WGRC

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

    Google Scholar 

  • Yu, A., Zhao, C., Fan, Y., Jang, W., Mungall, A.J., Deloukas, P., Olsen, A., Doggett, N.A., Ghebranious, N., Broman, K.W. and Weber, J.L. 2001. Comparison of human genetic and sequence-based physical maps. Nature 409: 951-953.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boyko, E., Kalendar, R., Korzun, V. et al. A high-density cytogenetic map of the Aegilops tauschii genome incorporating retrotransposons and defense-related genes: insights into cereal chromosome structure and function. Plant Mol Biol 48, 767–789 (2002). https://doi.org/10.1023/A:1014831511810

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1014831511810

Navigation