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A novel class of Helitron- related transposable elements in maize contain portions of multiple pseudogenes

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Abstract

We recently described a maize mutant caused by an insertion of a Helitron type transposable element (Lal, S.K., Giroux, M.J., Brendel, V., Vallejos, E. and Hannah, L.C., 2003, Plant Cell, 15: 381–391). Here we describe another Helitron insertion in the barren stalk1 gene of maize. The termini of a 6525 bp insertion in the proximal promoter region of the mutant reference allele of maize barren stalk1 gene (ba1-ref) shares striking similarity to the Helitron insertion we reported in the Shrunken-2 gene. This insertion is embedded with pseudogenes that differ from the pseudogenes discovered in the mutant Shrunken-2 insertion. Using the common terminal ends of the mutant insertions as a query, we discovered other Helitron insertions in maize BAC clones. Based on the comparison of the insertion site and PCR amplified genomic sequences, these elements inserted between AT dinucleotides. These putative non-autonomous Helitroninsertions completely lacked sequences similar to RPA (replication protein A) and DNA Helicases reported in other species. A blastn analysis indicated that both the 5′ and 3′ termini of Helitrons are repeated in the maize genome. These data provide strong evidence that Helitron type transposable elements are active and may have played an essential role in the evolution and expansion of the maize genome.

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References

  • S.F. Altschul W. Gish W. Miller E.W. Myers D.J. Lipman (1990) ArticleTitleBasic local alignment search tool J. Mol. Biol. 215 403–410

    Google Scholar 

  • J.L. Bennetzen (2000) ArticleTitleTransposable element contributions to plant gene and genome evolution Plant Mol. Biol. 42 251–269

    Google Scholar 

  • J.L. Bennetzen W. Ramakrishna (2002) ArticleTitleExceptional haplotype variation in maize Proc. Natl. Acad. Sci. USA 99 9093–9095

    Google Scholar 

  • V. Brendel W. Zhu (2002) ArticleTitleComputational modeling of gene structure in Arabidopsis thaliana Plant Mol. Biol. 48 49–58

    Google Scholar 

  • N. Collins J. Drake M. Ayliffe Q. Sun J. Ellis S. Hulbert T. Pryor (1999) ArticleTitleMolecular characterization of the maize Rp1-D rust resistance haplotype and its mutants Plant Cell 11 1365–1376 Occurrence Handle10.1105/tpc.11.7.1365 Occurrence Handle1:CAS:528:DyaK1MXkvFertbY%3D Occurrence Handle10402435

    Article  CAS  PubMed  Google Scholar 

  • H.P. Doring P. Starlinger (1986) ArticleTitleMolecular genetics of transposable elements in plants Annu. Rev. Genet. 20 175–200

    Google Scholar 

  • N.A. Eckardt (2003) ArticleTitleA new twist on transposon: the maize genome harbors a Helitron insertion Plant Cell 15 293–295

    Google Scholar 

  • W.R. Engels (1983) ArticleTitleThe P family of transposable elements in Drosophila Annu. Rev. Genet. 17 315–344

    Google Scholar 

  • Fedoroff N.V. (1989). In: Berg D.E., Howe M.M. (eds.), Mobile DINA American Society for Microbiology Press, Washington DC. PP. 375–411

  • N.V. Fedoroff (1989) ArticleTitleAbout maize transposable elements and development Cell 56 181–191

    Google Scholar 

  • C. Feschotte N. Jiang S.R. Wessler (2002) ArticleTitlePlant transposable elements: where genetics meets genomics Nat. Rev. Genet. 3 329–341

    Google Scholar 

  • C. Feschotte S.R. Wessler (2001) ArticleTitleTreasures in the attic: Rolling circle transposons discovered in eucaryotic genomes Proc. Natl. Acad. Sci. USA 98 8923–8914

    Google Scholar 

  • H. Fu H.K. Dooner (2002) ArticleTitleIntraspecific violation of genetic colinearity and its implications in maize Proc. Natl. Acad. Sci. USA 99 9573–9578

    Google Scholar 

  • A. Gallavotti Q. Zhao J. Kyozuka R. Meeley M. Ritter J. Doebley M. Enrico Pe‘ R.J. Schmidt (2004) ArticleTitleThe role of barren stalk1 in the architecture of maize Nature 132 630–635

    Google Scholar 

  • M.J. Giroux L.C. Hannah (1994) ArticleTitleADP-glucose pyrophosphorylase in shrunken2 and brittle2 mutants of maize Mol. Gen. Genet. 243 400–408

    Google Scholar 

  • X. Gong S. Kaushal E. Ceccarelli N. Bogdanova C. Neville T. Nguyen H. Clark Z.A. Khatib M. Valentine A.T. Look N. Rosenthal (1997) ArticleTitleDevelopmental regulation of Zbu1, a DNA-binding member of the SWI2/SNF2 family Dev. Biol. 183 166–182

    Google Scholar 

  • R.M. Hall C.M. Collis (1995) ArticleTitleMobile gene cassettes and integrons: capture and spread of genes by site-specific recombination Mol. Microbiol. 15 593–600

    Google Scholar 

  • Hofmeyer J.D.J. (1930). The inheritance and linkage relationships of barrenstalk1 and barrenstalk2, two mature plant characters of maize. Ph.D. Dissertation, Cornell University, Ithaca, New York, USA

  • Y.K. Jin J.L. Bennetzen (1989) ArticleTitleStructure and coding properties of Bs1, a maize retrovirus- like transposable element Proc Natl Acad Sci USA. 86 6235–6239

    Google Scholar 

  • V.V. Kapitonov J. Jurka (2001) ArticleTitleRolling circle transposons in eukaryotes Proc. Natl. Acad. Sci. USA 17 8714–8719

    Google Scholar 

  • V.V. Kapitonov J. Jurka (2003) ArticleTitleMolecular paleontology of transposable elements in the Drosophila melanogaster genome Proc. Natl. Acad. Sci. USA 100 6569–6574

    Google Scholar 

  • S.A. Khan (2000) ArticleTitlePlasmid rolling circle replication: recent development Mol. Microl. 37 477–484

    Google Scholar 

  • R. Kunze H. Saedler W.E. Lonnig (1997) ArticleTitlePlant transposable elements Adv. Bot. Res. 27 331–470

    Google Scholar 

  • S.K. Lal M.J. Giroux V. Brendel E. Vallejos L.C. Hannah (2003) ArticleTitleThe maize genome contains a Helitron insertion Plant Cell 15 381–391

    Google Scholar 

  • E.S. Lander et al. (2001) ArticleTitleInitial sequencing and analysis of the human genome Nature. 409 860–921

    Google Scholar 

  • C.J. Lawrence Q. Dong M.L. Polacco T.E. Seigfried V. Brendel (2004) ArticleTitleMaizeGDB, the community database for’ maize genetics and genomics Nucleic. Acids Res. 32 393–397

    Google Scholar 

  • C. Levesque S. Brassard J. Lapointe P.H. Roy (1994) ArticleTitleDiversity and relative strength of tandem promoters for the antibiotic-resistance genes of several integrons Gene 142 49–54 Occurrence Handle10.1016/0378-1119(94)90353-0 Occurrence Handle8181756

    Article  PubMed  Google Scholar 

  • D.R. McCarty (1986) ArticleTitleA simple method for extraction of RNA’from maize tissue Maize Genet. Coop. Newslett. 60 61

    Google Scholar 

  • M.V. Mendiola I. Bernales F. Cruz Particlede la (1994) ArticleTitleDifferential roles of the transposon termini in IS91 transposition Proc. Natl. Acad. Sci. (USA) 91 1922–1926

    Google Scholar 

  • P. Nevers N. Shepherd H. Saedler (1986) ArticleTitlePlant transposble elements Adv. Bot. Res. 12 102–203

    Google Scholar 

  • R.T. Poulter T.J. Goodwin M.I. Butler (2003) ArticleTitleVertebrate helentrons and other novel Helitrons Gene 313 201–212

    Google Scholar 

  • W. Ramakrishna J. Emberton M. Ogden P. SanMiguel J.L. Bennetzen (2002) ArticleTitleStructural analysis of the maize Rp1 complex reveals numerous sites and unexpected mechanisms of local rearrangement Plant Cell 13 3213–3223

    Google Scholar 

  • M.K. Ritter C.M. Padilla R.J. Schmidt (2002) ArticleTitleThe maize mutant barren stalk1 is defective in axillary meristem development Am. J. Bot. 89 203–210

    Google Scholar 

  • D.A. Rowe-Magnus D. Mazel (2001) ArticleTitleIntegrons: natural tools for bacterial genome evolution Curr. Opin. Microbiol. 5 565–569

    Google Scholar 

  • M.A. Saghai-Maroof K.M. Soliman R.A. Jorgensen R.W. Allard (1984) ArticleTitleRibosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics Proc. Natl. Acad. Sci. USA 81 8014–8018

    Google Scholar 

  • M.F. Singer V. Krek J.P. McMillan G.D. Swergold R.E. Thayer (1993) ArticleTitleLINE-1: a human transposable element Gene 135 183–188

    Google Scholar 

  • R. Song J. Messing (2003) ArticleTitleGene expression of a gene family in maize based on noncollinear haplotypes Proc. Natl. Acad. Sci. USA 100 9055–9060

    Google Scholar 

  • N. Tavakoli A. Comanducci H.M. Dodd M.C. Lett P. Albiger Bennett (2000) ArticleTitleIS1294, a DNA element that transposes by RC transposition Plasmid 44 66–84

    Google Scholar 

  • J. Usuka V. Brendel (2000) ArticleTitleGene structure prediction by spliced alignment of genomic DNA with protein sequences: increased accuracy by differential splice site scoring J. Mol. Biol. 297 1075–1085

    Google Scholar 

  • J. Usuka W. Zhu V. Brendel (2000) ArticleTitleOptimal spliced alignment of homologous cDNA to a genomic DNA template Bioinformatics 16 203–211

    Google Scholar 

  • S.R. Wessler T.E. Bureau S.E. White (1995) ArticleTitleLTR-retrotransposons and MITEs: Important players in the evolution of plant genomes Curr. Open. Genet. Dev. 5 814–821

    Google Scholar 

  • W. Zhu V. Brendel (2002) ArticleTitleGene structure identification with MyGV using cDNA evidence and protein homologs to improve al binitio predictions Bioinformatics 18 761–762

    Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, Oakland University, Rochester, MI, 48309-4401, USA

    Smriti Gupta, Gabrielle A. Stryker & Shailesh K. Lal

  2. Department of Biology, University of California, San Diego, La Jolla, 92093-0116, USA

    Andrea Gallavotti & Robert J. Schmidt

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  1. Smriti Gupta
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  2. Andrea Gallavotti
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  3. Gabrielle A. Stryker
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  4. Robert J. Schmidt
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  5. Shailesh K. Lal
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Correspondence to Shailesh K. Lal.

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Gupta, S., Gallavotti, A., Stryker, G.A. et al. A novel class of Helitron- related transposable elements in maize contain portions of multiple pseudogenes. Plant Mol Biol 57, 115–127 (2005). https://doi.org/10.1007/s11103-004-6636-z

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  • DOI: https://doi.org/10.1007/s11103-004-6636-z

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