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BoS: A Large and Diverse Family of Short Interspersed Elements (SINEs) in Brassica oleracea

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Abstract

Short interspersed elements (SINEs) are nonautonomous non-LTR retrotransposons that populate eukaryotic genomes. Numerous SINE families have been identified in animals, whereas only a few have been described in plants. Here we describe a new family of SINEs, named BoS, that is widespread in Brassicaceae and present at ∼2000 copies in Brassica oleracea. In addition to sharing a modular structure and target site preference with previously described SINEs, BoS elements have several unusual features. First, the head regions of BoS RNAs can adopt a distinct hairpin-like secondary structure. Second, with 15 distinct subfamilies, BoS represents one of the most diverse SINE families described to date. Third, several of the subfamilies have a mosaic structure that has arisen through the exchange of sequences between existing subfamilies, possibly during retrotransposition. Analysis of BoS subfamilies indicate that they were active during various time periods through the evolution of Brassicaceae and that active elements may still reside in some Brassica species. As such, BoS elements may be a valuable tool as phylogenetic makers for resolving outstanding issues in the evolution of species in the Brassicaceae family.

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References

  • P Capy C Bazin D Higuet T Langin (1998) Dynamics and evolution of transposable elements. Springer-Verlag Austin, TX

    Google Scholar 

  • JM Deragon BS Landry T Pelissier S Tutois S Tourmente G Picard (1994) ArticleTitleAn analysis of retroposition in plants based on a family of SINEs from Brassica napus J Mol Evol 39 378–86 Occurrence Handle10.1007/BF00160270 Occurrence Handle1:CAS:528:DyaK2cXmslemt7c%3D Occurrence Handle7966368

    Article  CAS  PubMed  Google Scholar 

  • M Dewannieux C Esnault T Heidmann (2003) ArticleTitleLINE-mediated retrotransposition of marked Alu sequences Nat Genet 35 41–48 Occurrence Handle1:CAS:528:DC%2BD3sXmslemu70%3D Occurrence Handle12897783

    CAS  PubMed  Google Scholar 

  • RF Doolittle D-F Feng Ms Johnson MA McClure (1989) ArticleTitleOrigins and evolutionary relationships of retroviruses Q Rev Biol 64 1–30 Occurrence Handle1:STN:280:BiaB387lsFY%3D Occurrence Handle2469098

    CAS  PubMed  Google Scholar 

  • TH Eickbush (1992) ArticleTitleTransposing without ends: the non-LTR retrotransposable elements New Biol 4 430–440 Occurrence Handle1:CAS:528:DyaK38Xmt1Oitrg%3D Occurrence Handle1325183

    CAS  PubMed  Google Scholar 

  • IL Hofacker (2003) ArticleTitleVienna RNA secondary structure server Nucleic Acids Res 31 3429–3431 Occurrence Handle1:CAS:528:DC%2BD3sXltVWisrs%3D Occurrence Handle12824340

    CAS  PubMed  Google Scholar 

  • J Jurka (1997) ArticleTitleSequence patterns indicate an enzymatic involvement in integration of mammalian retroposons Proc Natl Acad Sci USA 94 1872–1877 Occurrence Handle10.1073/pnas.94.5.1872 Occurrence Handle1:CAS:528:DyaK2sXhslaqtLo%3D Occurrence Handle9050872

    Article  CAS  PubMed  Google Scholar 

  • P Kachroo SA Leong BB Chattoo (1995) ArticleTitleMg-SINE: a short interspersed nuclear element from the rice blast fungus, Magnaporthe grisea Proc Natl Acad Sci USA 92 11125–11129 Occurrence Handle1:CAS:528:DyaK2MXps1alsbw%3D Occurrence Handle7479950

    CAS  PubMed  Google Scholar 

  • M Kajikawa N Okada (2002) ArticleTitleLINEs mobilize SINEs in the eel through a shared 3′ sequence Cell 111 433–444 Occurrence Handle1:CAS:528:DC%2BD38XovVaku7k%3D Occurrence Handle12419252

    CAS  PubMed  Google Scholar 

  • DH Kass MA Batzer PL Deininger (1995) ArticleTitleGene conversion as a secondary mechanism of short interspersed element (SINE) evolution Mol Cell Biol 15 19–25 Occurrence Handle1:CAS:528:DyaK2MXislamsL8%3D Occurrence Handle7799926

    CAS  PubMed  Google Scholar 

  • D Labuda E Zietkiewicz (1994) ArticleTitleEvolution of secondary structure in the family of 7SL-like RNAs J Mol Evol 39 506–518 Occurrence Handle1:CAS:528:DyaK2MXhvF2hur4%3D Occurrence Handle7528809

    CAS  PubMed  Google Scholar 

  • D Labuda D Sinnett C Richer JM Deragon G Striker (1991) ArticleTitleEvolution of mouse B1 repeats: 7SL RNA folding pattern conserved J Mol Evol 32 405–414 Occurrence Handle1:CAS:528:DyaK3MXisVWrtr8%3D Occurrence Handle1710278

    CAS  PubMed  Google Scholar 

  • ES Lander LM Linton B Birren C Nusbaum MC Zody J, Baldwin et al. (2001) ArticleTitleInitial sequencing and analysis of the human genome Nature 409 860–921 Occurrence Handle10.1038/35057062 Occurrence Handle11237011

    Article  PubMed  Google Scholar 

  • A Lenoir B Cournoyer S Warwick G Picard JM Deragon (1997) ArticleTitleEvolution of SINE S1 retroposons in Cruciferae plant species Mol Biol Evol 14 934–941 Occurrence Handle1:CAS:528:DyaK2sXlvVejurY%3D Occurrence Handle9287426

    CAS  PubMed  Google Scholar 

  • A Lenoir L Lavie JL Prieto C Goubely JC Cote T Pelissier JM Deragon (2001) ArticleTitleThe evolutionary origin and genomic organization of SINEs in Arabidopsis thaliana Mol Biol Evol 18 2315–2322 Occurrence Handle1:CAS:528:DC%2BD3MXptFCrsLc%3D Occurrence Handle11719581

    CAS  PubMed  Google Scholar 

  • TM Lowe SR Eddy (1997) ArticleTitletRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence Nucleic Acids Res 25 955–964 Occurrence Handle1:CAS:528:DyaK2sXhvVahtrk%3D Occurrence Handle9023104

    CAS  PubMed  Google Scholar 

  • DD Luan MH Korman JL Jakubczak TH Eickbush (1993) ArticleTitleReverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition Cell 72 595–605 Occurrence Handle1:CAS:528:DyaK3sXhs1ansrc%3D Occurrence Handle7679954

    CAS  PubMed  Google Scholar 

  • R Muddashetty T Khanam A Kondrashov M Bundman A Iacoangeli J Kremerskothen K Duning A Barnekow A Huttenhofer H Tiedge J Brosius (2002) ArticleTitlePoly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles J Mol Biol 321 433–445 Occurrence Handle1:CAS:528:DC%2BD38XlvF2hu70%3D Occurrence Handle12162957

    CAS  PubMed  Google Scholar 

  • F Myouga S Tsuchimoto K Noma H Ohtsubo E Ohtsubo (2001) ArticleTitleIdentification and structural analysis of SINE elements in the Arabidopsis thaliana genome Genes Genet Syst 76 169–179 Occurrence Handle1:CAS:528:DC%2BD3MXntFagtLc%3D Occurrence Handle11569500

    CAS  PubMed  Google Scholar 

  • I Ogiwara M Miya K Ohshima N Okada (1999) ArticleTitleRetropositional parasitism of SINEs on LINEs: identification of SINEs and LINEs in elasmobranchs Mol Biol Evol 16 1238–1250 Occurrence Handle1:CAS:528:DyaK1MXmtVWntbY%3D Occurrence Handle10486979

    CAS  PubMed  Google Scholar 

  • K Ohshima R Koishi M Matsuo N Okada (1993) ArticleTitleSeveral short interspersed repetitive elements (SINEs) in distant species may have originated from a common ancestral retrovirus: characterization of a squid SINE and a possible mechanism for generation of tRNA-derived retroposons Proc Natl Acad Sci USA 90 6260–6264 Occurrence Handle1:CAS:528:DyaK3sXltlaks7o%3D Occurrence Handle8327507

    CAS  PubMed  Google Scholar 

  • K Ohshima M Hamada Y Terai N Okada (1996) ArticleTitleThe 3′ ends of tRNA-derived short interspersed repetitive elements are derived from the 3′ ends of long interspersed repetitive elements Mol Cell Biol 16 3756–3764 Occurrence Handle1:CAS:528:DyaK28XjvVWnurg%3D Occurrence Handle8668192

    CAS  PubMed  Google Scholar 

  • N Okada (1991a) ArticleTitleSINEs Curr Opin Genet Dev 1 498–504 Occurrence Handle1:CAS:528:DyaK38XhvVylurs%3D

    CAS  Google Scholar 

  • N Okada (1991b) ArticleTitleSINEs: short interspersed repeated elements of the eukaryotic genome Trends Ecol Evol 6 358–361

    Google Scholar 

  • N Okada M Hamada (1997) ArticleTitleThe 3′ ends of tRNA-derived SINEs originated from the 3′ ends of LINEs: a new example from the bovine genome J Mol Evol 44 S52–S56 Occurrence Handle1:CAS:528:DyaK2sXhsFGrsbY%3D Occurrence Handle9071012

    CAS  PubMed  Google Scholar 

  • N Okada M Hamada I Ogiwara K Ohshima (1997) ArticleTitleSINEs and LINEs share common 3′ sequences: a review Gene 205 229–243 Occurrence Handle1:CAS:528:DyaK1cXmtlWitA%3D%3D Occurrence Handle9461397

    CAS  PubMed  Google Scholar 

  • TS Rozhdestvensky AM Kopylov J Brosius A Huttenhofer (2001) ArticleTitleNeuronal BC1 RNA structure: evolutionary conversion of a tRNA(Ala) domain into an extended stem-loop structure RNA 7 722–730 Occurrence Handle1:CAS:528:DC%2BD3MXjsVensb4%3D Occurrence Handle11350036

    CAS  PubMed  Google Scholar 

  • CW Schmid (1996) ArticleTitleAlu: structure, origin, evolution, significance and function of one-tenth of human DNA Prog Nucleic Acid Res Mol Biol 53 283–319 Occurrence Handle1:CAS:528:DyaK28XktlCms70%3D Occurrence Handle8650306

    CAS  PubMed  Google Scholar 

  • MR Shen MA Batzer PL Deininger (1991) ArticleTitleEvolution of the master Alu gene(s) J Mol Evol 33 311–320 Occurrence Handle1:CAS:528:DyaK3MXmtVShs7w%3D Occurrence Handle1774786

    CAS  PubMed  Google Scholar 

  • D Sinnett C Richer JM Deragon D Labuda (1991) ArticleTitleAlu RNA secondary structure consists of two independent 7 SL RNA-like folding units J Biol Chem 266 8675–8678 Occurrence Handle1:CAS:528:DyaK3MXkt1Clsr8%3D Occurrence Handle1709156

    CAS  PubMed  Google Scholar 

  • DL Swofford (1999) PAUP*: phylogenetic analysis using parsimony and other methods Sinauer Sunderland, MA

    Google Scholar 

  • K Takahashi N Okada (2002) ArticleTitleMosaic structure and retropositional dynamics during evolution of subfamilies of short interspersed elements in African cichlids Mol Biol Evol 19 1303–1312 Occurrence Handle1:CAS:528:DC%2BD38XmtF2rsro%3D Occurrence Handle12140242

    CAS  PubMed  Google Scholar 

  • C Tatout L Lavie JM Deragon (1998) ArticleTitleSimilar target site selection occurs in integration of plant and mammalian retroposons J Mol Evol 47 463–470 Occurrence Handle1:CAS:528:DyaK1cXms1Wlsb4%3D Occurrence Handle9767691

    CAS  PubMed  Google Scholar 

  • Y Terai K Takahashi N Okada (1998) ArticleTitleSINE cousins: the 3′ end tails of the two oldest and distantly related families of SINEs are descended from the 3′ ends of LINEs with the same genealogical origin Mol Biol Evol 15 1460–1471 Occurrence Handle1:CAS:528:DyaK1cXntlOgsrk%3D Occurrence Handle12572609

    CAS  PubMed  Google Scholar 

  • E Ullu C Tschudi (1984) ArticleTitleAlu sequences are processed 7SL RNA genes Nature 312 171–172 Occurrence Handle1:CAS:528:DyaL2MXktVymtw%3D%3D Occurrence Handle6209580

    CAS  PubMed  Google Scholar 

  • M Umeda H Ohtsubo E Ohtsubo (1991) ArticleTitleDiversification of the rice Waxy gene by insertion of mobile DNA elements into introns Jpn J Genet 66 569–586 Occurrence Handle1:CAS:528:DyaK38Xhs1Oks7o%3D Occurrence Handle1685658

    CAS  PubMed  Google Scholar 

  • AM Weiner (1980) ArticleTitleAn abundant cytoplasmic 7S RNA is complementary to the dominant interspersed middle repetitive DNA sequence family in the human genome Cell 22 209– 218 Occurrence Handle1:CAS:528:DyaL3MXhtlegsQ%3D%3D Occurrence Handle6159101

    CAS  PubMed  Google Scholar 

  • N West AM Roy-Engel H Imataka N Sonenberg P Deininger (2002) ArticleTitleShared protein components of SINE RNPs J Mol Biol 321 423–432 Occurrence Handle1:CAS:528:DC%2BD38XlvF2hur8%3D Occurrence Handle12162956

    CAS  PubMed  Google Scholar 

  • Y Xiong TH Eickbush (1990) ArticleTitleOrigin and evolution of retroelements based upon their reverse transcriptase sequences EMBOL J 9 3353–3362 Occurrence Handle1:CAS:528:DyaK3cXmt1Ghsbk%3D

    CAS  Google Scholar 

  • Y Yoshioka S Matsumoto S Kojima K Ohshima N Okada Y Machida (1993) ArticleTitleMolecular characterization of a short interspersed repetitive element from tobacco that exhibits sequence homology to specific tRNAs Proc Natl Acad Sci USA 90 6562–6566 Occurrence Handle1:CAS:528:DyaK3sXlsFeitb4%3D Occurrence Handle8341669

    CAS  PubMed  Google Scholar 

  • E Zietkiewicz D Labuda (1996) ArticleTitleMosaic evolution of rodent B1 elements J Mol Evol 42 66–72 Occurrence Handle1:CAS:528:DyaK28XntFOmtw%3D%3D Occurrence Handle8576966

    CAS  PubMed  Google Scholar 

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Acknowledgments

Preliminary sequence data were obtained from The Institute for Genomic Research Web site at http://www.tigr.org. Sequencing of Brassica oleracea was funded by the National Science Foundation. This work was supported by grants from the National Science Foundation and the National Institutes of Health to S.R.W.

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  1. Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA

    Xiaoyu Zhang & Susan R. Wessler

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  1. Xiaoyu Zhang
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  2. Susan R. Wessler
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Correspondence to Susan R. Wessler.

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Zhang, X., Wessler, S.R. BoS: A Large and Diverse Family of Short Interspersed Elements (SINEs) in Brassica oleracea. J Mol Evol 60, 677–687 (2005). https://doi.org/10.1007/s00239-004-0259-5

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