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A hAT superfamily transposase recruited by the cereal grass genome

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Abstract

Transposable elements are ubiquitous genomic parasites with an ancient history of coexistence with their hosts. A few cases have emerged recently where these genetic elements have been recruited for normal function in the host organism. We have identified an expressed hobo/Ac/Tam (hAT) family transposase-like gene in cereal grasses which appears to represent such a case. This gene, which we have called gary, is found in one or two copies in barley, two diverged copies in rice and two very similar copies in hexaploid wheat. No gary homologues are found in Arabidopsis. In all three cereal species, an apparently complete 2.5 kb transposase-like open reading frame is present and nucleotide substitution data show evidence for positive selection, yet the predicted gary protein is probably not an active transposase, as judged by the absence of key amino acids required for transposase function. Gary is expressed in wheat and barley spikes and gary cDNA sequences are also found in rice, oat, rye, maize, sorghum and sugarcane. The short inverted terminal repeats, flanked by an eight-nucleotide host sequence duplication, which are characteristic of a hAT transposon are absent. Genetic mapping in barley shows that gary is located on the distal end of the long arm of chromosome 2H. Wheat homologues of gary map to the same approximate location on the wheat group 2 chromosomes by physical bin-mapping and the more closely related of the two rice garys maps to the syntenic location near the bottom of rice chromosome 4. These data suggest that gary has resided in a single genomic location for at least 60 Myr and has lost the ability to transpose, yet expresses a transposase-related protein that is being conserved under host selection. We propose that the gary transposase-like gene has been recruited by the cereal grasses for an unknown function.

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References

  • Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751

    Article  PubMed  CAS  Google Scholar 

  • Biessmann H, Champion LE, O’Hair M, Ikenaga K, Kasravi B, Mason JM (1992) Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J 11:4459–4469

    PubMed  CAS  Google Scholar 

  • Bundock P, Hooykaas P (2005) An Arabidopsis hAT-like transposase is essential for plant development. Nature 436:282–284

    Article  PubMed  CAS  Google Scholar 

  • Caldwell DG, McCallum N, Shaw P, Muehlbauer GJ, Marshall DF, Waugh R (2004) A structured mutant population for forward and reverse genetics in barley (Hordeum vulgare L.). Plant J 40:143–150

    Article  PubMed  CAS  Google Scholar 

  • Calvi BR, Hong TJ, Findley SD, Gelbart WM (1991) Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator and Tam3. Cell 66:465–471

    Article  PubMed  CAS  Google Scholar 

  • Chalhoub B, Allouis Safá J, Janda J, Bellec A, Sarda X, Arar C, Lefèvre A, Rouault P, Pateyron S, Dupin A, Burgio G, Georget C, Sourdille P, Faivre-Rampant, P, Caboche M, Moore G, Bernard M, Doleel J (2003) Towards precise analysis of the wheat genome: preparation of genomic resources for structural and functional characterization. In: Proceedings of the tenth international wheat genetic symposium, Paestum, Italy, September 1–6, 2003.

  • Chantret N, Salse J, Sabot F, Rahman S, Bellec A et al (2005) Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (triticum and aegilops). Plant Cell 17:1033–1045

    Article  PubMed  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Article  PubMed  CAS  Google Scholar 

  • Conley EJ, Nduati V, Gonzalez-Hernandez JL, Mesfin A, Trudeau-Spanjers M et al (2004) A 2600-locus chromosome bin map of wheat homoeologous group 2 reveals interstitial gene-rich islands and colinearity with rice. Genetics 168:625–637

    Article  PubMed  CAS  Google Scholar 

  • Craig NL, Craigie R, Gellert M, Lambowitz A (eds) (2002) Mobile DNA II. American Society for Microbiology Press

  • Essers L, Adolphs RH, Kunze R (2000) A highly conserved domain of the maize activator transposase is involved in dimerization. Plant Cell 12:211–224

    Article  PubMed  CAS  Google Scholar 

  • Federoff N, Wessler S, Shure M (1983) Isolation of the transposable maize controlling elements Ac and Ds. Cell 35:235–242

    Article  PubMed  Google Scholar 

  • Finnegan DH (1990) Transposable elements and DNA transposition in eukaryotes. Curr Opin Cell Biol 2:471–477

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Voytas DF (2005) A eukaryotic gene family related to retroelement integrases. Trends Genet 21:133–137

    Article  PubMed  CAS  Google Scholar 

  • Hartl DL, Lohe AR, Lozovskaya ER (1997) Modern thoughts on an ancient mariner: function, evolution, regulation. Annu Rev Genet 31:337–358

    Article  PubMed  CAS  Google Scholar 

  • Healey J, Corr C, Deyoung J, Baker B (1993) Linked and unlinked transposition of a genetically marked Dissociation element in transgenic tomato. Genetics 134:571–584

    PubMed  Google Scholar 

  • Hehl R, Baker B (1989) Induced transposition of Ds by a stable Ac in crosses of transgenic tobacco plants. Mol Gen Genet 217:53–59

    Article  PubMed  CAS  Google Scholar 

  • Hudson ME, Lisch DR, Quail PH (2003) The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signalling pathway. Plant J 34:453–471

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2004) Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biol 23:311–324

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2005) RAG1core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3 e181:1–14

    Google Scholar 

  • Kunze R, Saedler H, Lonnig WE (1997) Plant transposable elements. Adv Bot Res 27:331–469

    Article  CAS  Google Scholar 

  • Levis RW, Ganesan R, Houtchens K, Tolar LA, Sheen FM (1993) Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75:1083–1093

    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 

  • Lynch C, Tristem M (2003) A co-opted gypsy-type LTR-retrotransposon is conserved in the genomes of humans, sheep, mice and rats. Curr Biol 13:1518–1523

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1948) Mutable loci in maize. Carnegie Inst Washington Yearbook 47:155–169

    Google Scholar 

  • McClintock B (1951) Chromosome organisation and genic expression. Cold Spring Harbor Symp Quant Biol 16:13–47

    PubMed  CAS  Google Scholar 

  • Moore G, Devos KM, Wang Z, Gale MD (1995) Grasses line up and form a circle. Curr Biol 5:737

    Article  PubMed  CAS  Google Scholar 

  • de la Pena RC, Smith KP, Capettini F, Muehlbauer GJ, Gallo-Meagher M, Dill-Macky R, Somers DA, Ramusson DC (1999) Quantitative trait loci associated with resistance to Fusarium head blight and kernel discoloration in barley. Theor Appl Genet 99:561–569

    Article  Google Scholar 

  • Rio DC (1990) Molecular mechanisms regulating Drosophila P element transposition. Annu Rev Genet 24:543–578

    Article  PubMed  CAS  Google Scholar 

  • Rostoks N, Mudie S, Cardle L, Russell J, Ramsay L et al (2005) Genome-wide SNP discovery and linkage analysis in barley based on genes responsive to abiotic stress. Mol Genet Genomics (in press)

  • Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Smith KP, Evans CK, Dill-Macky R, Gustus C, Yie W, Dong Y (2004) Host effect on deoxynivalenol accumulation in Fusarium head blight of barley. Phytopathology 94:766–771

    Article  CAS  PubMed  Google Scholar 

  • Sorrels ME, La Rota M, Bermudez-Kandianis CE, Greene RA, Kantety R et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827

    PubMed  Google Scholar 

  • Sundararajan P, Atkinson PW, O’Brochta DA (1999) Transposable element interactions in insects: crossmobilization of hobo and Hermes. Insect Mol Biol 8:359–368

    Article  PubMed  CAS  Google Scholar 

  • Thomas WTB, Baird E, Fuller JD, Lawrence P, Young G, Russell JR, Ramsay L, Waugh R, Powell W (1998) Identification of a QTL decreasing yield in barley linked to Mlo powdery mildew resistance. Mol Breeding 4:381–393

    Article  CAS  Google Scholar 

  • Wessler SR (1996) Turned on by stress. Curr Biol 6:959–961

    Article  PubMed  CAS  Google Scholar 

  • Xu Z, Dooner HK (2005) Mx-rMx, a family of interacting transposons in the growing hAT superfamily of maize. Plant Cell 17:375–388

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Zhou J et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3 e38:0266-0281

    Google Scholar 

  • Zhou L, Mitra R, Atkinson PW, Burgess Hickman A, Dyda F, Craig NL (2004) Transposition of hAT elements links transposable elements and V(D)J recombination. Nature 432:995–1001

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

GJM was supported by a McKnight Landgrant Professorship for sabbatical leave to the Scottish Crop Research Institute. BSB was supported by a Boyscast Fellowship from the Indian government. We thank Maggie Knox for help with performing K s/K a determinations, the Genoplante consortium (http://www.genoplante.com) for making available the hexaploid BAC library, Emily Conley and Jim Anderson for help with deletion mapping and Robbie Waugh and Noel Ellis for many useful discussions.

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Correspondence to Andrew J. Flavell.

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Communicated by M.-A. Grandbastien

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Muehlbauer, G.J., Bhau, B.S., Syed, N.H. et al. A hAT superfamily transposase recruited by the cereal grass genome. Mol Genet Genomics 275, 553–563 (2006). https://doi.org/10.1007/s00438-006-0098-8

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