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The Genomic Organization of Retrotransposons in Brassica oleracea

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Abstract

We have investigated the copy numbers and genomic organization of five representative reverse transcriptase domains from retrotransposons in Brassica oleracea. Two non-homologous Pseudoviridae (Ty1/copia-like) elements, two Metaviridae (Ty3/gypsy-like) elements (one related to the Athila family) and one Retroposinae (LINE) element were hybridized to a gridded BAC library, “BoB”. The results indicated that the individual LTR retrotransposons (copia and gypsy-like) were represented by between 90 and 320 copies in the haploid genome, with only evidence of a single location for the LINE. Sequence analysis of the same elements against genome survey sequence gave estimates of between 60 and 570, but no LINE was found. There was minimal evidence for clustering between any of these retroelements: only half the randomly expected number of BACs hybridized to both LTR-retrotransposon families. Fluorescent in situ hybridization showed that each of the retroelements had a characteristic genomic distribution. Our results suggest there are preferential sites and perhaps control mechanisms for the insertion or excision of different retrotransposon groups.

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References

  • K. Alix J.S. Heslop-Harrison (2004) ArticleTitleThe diversity of retroelements in diploid and allotetraploid Brassica species Plant Mol. Biol. 54 895–909 Occurrence Handle10.1007/s11103-004-0391-z Occurrence Handle15612105 Occurrence Handle1:CAS:528:DC%2BD2cXhtVGjurnP

    Article  PubMed  CAS  Google Scholar 

  • O.D. Anderson C. Rausch O. Moullet E.S. Lagudah (2003) ArticleTitleThe wheat D-genome HMW-glutenin locus: BAC sequencing, gene distribution, and retrotransposon clusters Funct. Integr. Genomics 3 56–68 Occurrence Handle12590343 Occurrence Handle1:CAS:528:DC%2BD3sXht1CktLs%3D

    PubMed  CAS  Google Scholar 

  • InstitutionalAuthorNameThe Arabidopsis Genome Initiative (2000) ArticleTitleAnalysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature 108 796–815

    Google Scholar 

  • D. Babula M. Kaczmarek A. Barakat M. Delseny C.F. Quiros J. Sadowski (2003) ArticleTitleChromosomal mapping of Brassica oleracea based on ESTs from Arabidopsis thaliana: complexity of the comparative map Mol. Gen. Genomics 268 656–665 Occurrence Handle1:CAS:528:DC%2BD3sXhtFSmsbs%3D

    CAS  Google Scholar 

  • A. Belyayev O. Raskina E. Nevo (2001) ArticleTitleChromosomal distribution of reverse transcriptase-containing retroelements in two Triticeae species Chromosome Res. 9 129–136 Occurrence Handle10.1023/A:1009231019833 Occurrence Handle11321368 Occurrence Handle1:CAS:528:DC%2BD3MXislaqtbw%3D

    Article  PubMed  CAS  Google Scholar 

  • A. Benabdelmouna H. Darmency (2003) ArticleTitleCopia-like retrotransposons in the genus Setaria: Sequence heterogeneity, species distribution and chromosomal organization Plant Syst. Evol. 237 127–136 Occurrence Handle10.1007/s00606-002-0250-9 Occurrence Handle1:CAS:528:DC%2BD3sXjtVehsrk%3D

    Article  CAS  Google Scholar 

  • A. Brandes J.S. Heslop-Harrison A. Kamm S. Kubis R.L. Doudrick T. Schmidt (1997) ArticleTitleComparative analysis of the chromosomal and genomic organization of Ty1-copia like retrotransposons in pteridophytes, gymnosperms and angiosperms Plant Mol. Biol. 33 11–21 Occurrence Handle10.1023/A:1005797222148 Occurrence Handle9037155 Occurrence Handle1:CAS:528:DyaK2sXhsVegs78%3D

    Article  PubMed  CAS  Google Scholar 

  • A.C. Cavell D.J. Lydiate I.A. Parkin C. Dean M. Trick (1998) ArticleTitleCollinearity between a 30-centimorgan segment of Arabidopsis thaliana chromosome 4 and duplicated regions within the Brassica napus genome Genome 41 62–69 Occurrence Handle10.1139/gen-41-1-62 Occurrence Handle9549059 Occurrence Handle1:CAS:528:DyaK1cXisVChu7o%3D

    Article  PubMed  CAS  Google Scholar 

  • Z. Cheng G.G. Presting C. Robin Buell R.A. Wing J. Jiang (2001) ArticleTitleHigh-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice Genetics 157 1749–1757 Occurrence Handle11290728 Occurrence Handle1:CAS:528:DC%2BD3MXjsFemtb0%3D

    PubMed  CAS  Google Scholar 

  • A.-M. Chèvre F. Eber A. Baranger M. Renard (1997) ArticleTitleGene flow from transgenic crops Nature 389 924

    Google Scholar 

  • A. Fiebig R. Kimport D. Preuss (2004) ArticleTitleComparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification Proc. Natl. Acad. Sci. USA 101 3286–3291 Occurrence Handle14970339 Occurrence Handle1:CAS:528:DC%2BD2cXitlWhu74%3D

    PubMed  CAS  Google Scholar 

  • A.J. Flavell D.B. Smith A. Kumar (1992) ArticleTitleExtreme heterogeneity of Ty1-copia group retrotransposons in plants Mol. Gen. Genet. 231 233–242 Occurrence Handle1370976 Occurrence Handle1:CAS:528:DyaK38XkvVCnsbc%3D

    PubMed  CAS  Google Scholar 

  • A.J. Flavell M.R. Knox S.R. Pearce T.H.N. Ellis (1998) ArticleTitleRetrotransposon-based insertion polymorphisms (RBIP) for high throughput marker analysis Plant J. 16 643–650 Occurrence Handle10.1046/j.1365-313x.1998.00334.x Occurrence Handle10036780 Occurrence Handle1:CAS:528:DyaK1MXovVSntQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • M.G. Francki (2001) ArticleTitleIdentification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.) Genome 44 266–274 Occurrence Handle10.1139/gen-44-2-266 Occurrence Handle11341737 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Srurk%3D

    Article  PubMed  CAS  Google Scholar 

  • P. Fransz S. Armstrong C. Alonso-Blanco T.C. Fischer R.A. Torres-Ruiz G. Jones (1998) ArticleTitleCytogenetics for the model system Arabidopsis thaliana Plant J. 13 867–876 Occurrence Handle10.1046/j.1365-313X.1998.00086.x Occurrence Handle9681023 Occurrence Handle1:CAS:528:DyaK1cXislejsb4%3D

    Article  PubMed  CAS  Google Scholar 

  • N. Friesen A. Brandes J.S. Heslop-Harrison (2001) ArticleTitleDiversity, origin, and distribution of retrotransposons (gypsy and copia) in conifers Mol. Biol. Evol. 18 1176–1188 Occurrence Handle11420359 Occurrence Handle1:CAS:528:DC%2BD3MXltVGrurw%3D

    PubMed  CAS  Google Scholar 

  • H Fu W Park X Yan Z Zheng B Shen K. Dooner (2001) ArticleTitleThe highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome Proc. Natl. Acad. Sci. USA 98 8903–8908 Occurrence Handle11438686 Occurrence Handle1:CAS:528:DC%2BD3MXls1Wiu7g%3D

    PubMed  CAS  Google Scholar 

  • M. Gao G. Li B. Yang W.R. McCombie C.F. Quiros (2004) ArticleTitleComparative analysis of a Brassica BAC clone containing several major aliphatic glucosinolate genes with its corresponding Arabidopsis sequence Genome 47 666–679 Occurrence Handle10.1139/g04-021 Occurrence Handle15284871 Occurrence Handle1:CAS:528:DC%2BD2cXotlyks7w%3D

    Article  PubMed  CAS  Google Scholar 

  • Gish, W.R., 2005. WU-BLAST archives: http://blast.wustl.edu

  • G.E. Harrison J.S. Heslop-Harrison (1995) ArticleTitleCentromeric repetitive DNA in the genus Brassica Theor. Appl. Genet. 90 157–165 Occurrence Handle10.1007/BF00222197 Occurrence Handle1:CAS:528:DyaK2MXls1Cjsrc%3D

    Article  CAS  Google Scholar 

  • E.C. Howell G.C. Barker G.H. Jones M.J. Kearsey G.J. King E.P. Kop C.D. Ryder G.R. Teakle J.G. Vicente S.J. Armstrong (2002) ArticleTitleIntegration of the cytogenetic and genetic linkage maps of Brassica oleracea Genetics 161 1225–1234 Occurrence Handle12136025 Occurrence Handle1:CAS:528:DC%2BD38XmsF2qsr0%3D

    PubMed  CAS  Google Scholar 

  • S. Hudakova W. Michalek G.G. Presting R. ten Hoopen K. dos Santos Z. Jecencakova I. Schubert (2001) ArticleTitleSequence organization of barley centromeres Nucleic Acids Res. 29 5029–5035 Occurrence Handle10.1093/nar/29.24.5029 Occurrence Handle11812833 Occurrence Handle1:CAS:528:DC%2BD38XmslWgtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • S.P. Kowalski T.-H. Lan K.A. Feldmann A.H. Paterson (1994) ArticleTitleComparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization Genetics 138 499–510 Occurrence Handle7828831 Occurrence Handle1:CAS:528:DyaK2MXmtFaqs78%3D

    PubMed  CAS  Google Scholar 

  • A.G.J. Kuipers J.S. Heslop-Harrison E. Jacobsen (1998) ArticleTitleCharacterisation and physical localisation of Ty1-copia-like retrotransposons in four Alstroemeria species Genome 41 357–367 Occurrence Handle10.1139/gen-41-3-357 Occurrence Handle9729770 Occurrence Handle1:CAS:528:DyaK1cXlvVCrsLg%3D

    Article  PubMed  CAS  Google Scholar 

  • A. Kumar J.L. Bennetzen (1999) ArticleTitlePlant retrotransposons Annu. Rev. Genet. 33 479–532 Occurrence Handle10.1146/annurev.genet.33.1.479 Occurrence Handle10690416 Occurrence Handle1:CAS:528:DC%2BD3cXhtVSms7k%3D

    Article  PubMed  CAS  Google Scholar 

  • A. Kumar S.R. Pearce K. McLean G. Harrison J.S. Heslop-Harrison R. Waugh A.J. Flavell (1997) ArticleTitleThe Ty1-copia group of retrotransposons in plants: genomic organization, evolution, and use as molecular markers Genetica 100 205–217 Occurrence Handle10.1023/A:1018393931948 Occurrence Handle9440274 Occurrence Handle1:CAS:528:DyaK1cXkslWltA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • N. Kurata K.-I. Nonomura Y. Harushima (2002) ArticleTitleRice genome organization: the centromere and genome interactions Ann. Bot. 90 427–435 Occurrence Handle10.1093/aob/mcf218 Occurrence Handle12324265 Occurrence Handle1:CAS:528:DC%2BD38XovFWnsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • U. Lagercrantz (1998) ArticleTitleComparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements Genetics 150 1217–1228 Occurrence Handle9799273 Occurrence Handle1:CAS:528:DyaK1cXnsFCntb0%3D

    PubMed  CAS  Google Scholar 

  • U. Lagercrantz D. Lydiate (1996) ArticleTitleComparative genome mapping in Brassica Genetics 144 1903–1910 Occurrence Handle8978073 Occurrence Handle1:CAS:528:DyaK2sXkslylsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • L. Lavie J-L. Prieto C. Tatout J-M. Deragon (2002) ArticleTitleBali1A, a possible LINE partner for the SINE S1 in Brassica napus Genome letters 1 IssueID8 123–130 Occurrence Handle1:CAS:528:DC%2BD3sXmt1CrtLo%3D

    CAS  Google Scholar 

  • P.R.J. Leeton D.R. Smyth (1993) ArticleTitleAn abundant LINE-like element amplified in the genome of Lilium speciosum Mol. Gen. Genet. 237 97–104 Occurrence Handle10.1007/BF00282789 Occurrence Handle7681139 Occurrence Handle1:CAS:528:DyaK3sXisV2htb8%3D

    Article  PubMed  CAS  Google Scholar 

  • A.V. Lukashin M. Borodovsky (1998) ArticleTitleGeneMark.hmm: new solutions for gene finding Nucleic Acids Res. 25 955–964

    Google Scholar 

  • J.A. Mayfield A. Fiebig S.E. Johnstone D. Preuss (2001) ArticleTitleGene families from the Arabidopsis thaliana pollen coat proteome Science 292 2482–2485 Occurrence Handle10.1126/science.1060972 Occurrence Handle11431566 Occurrence Handle1:CAS:528:DC%2BD3MXkvFWmu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • A. Miura M. Kato K. Watanabe A. Kawabe H. Kotani T. Kakutani (2004) ArticleTitleGenomic localization of endogenous mobile CACTA family transposons in natural variants of Arabidopsis thaliana Mol. Gen. Genomics 270 524–532 Occurrence Handle10.1007/s00438-003-0943-y Occurrence Handle1:CAS:528:DC%2BD2cXlvFentA%3D%3D

    Article  CAS  Google Scholar 

  • R.J. Mroczek R.K. Dawe (2003) ArticleTitleDistribution of retroelements in centromeres and neocentromeres of maize Genetics 165 809–819 Occurrence Handle14573490 Occurrence Handle1:CAS:528:DC%2BD3sXpt1OlsLw%3D

    PubMed  CAS  Google Scholar 

  • C. O’Neill I. Bancroft (2000) ArticleTitleComparative physical mapping of segments of the genome of Brassica oleracea var. alboglabra that are homoeologous to sequenced regions of chromosomes 4 and 5 of Arabidopsis thaliana Plant J. 23 233–243 Occurrence Handle10929117 Occurrence Handle1:CAS:528:DC%2BD3cXmtFOnsLw%3D

    PubMed  CAS  Google Scholar 

  • T. Pélissier S. Tutois J.-M. Deragon S. Tourmente S. Genestier G. Picard (1995) ArticleTitleAthila, a new retroelement from Arabidopsis thaliana Plant Mol. Biol. 29 441–452 Occurrence Handle8534844

    PubMed  Google Scholar 

  • T. Pélissier S. Tutois S. Tourmente J.M. Deragon G. Picard (1996) ArticleTitleDNA regions flanking the major Arabidopsis thaliana satellite are principally enriched in Athila retroelement sequences Genetica 97 141–151 Occurrence Handle8984010

    PubMed  Google Scholar 

  • Peterson-Burch, B., Nettleton, D. and Voytas, D.F., 2004. Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae. Genome Biology 5(10), R78:http://genomebiology.com/2004/5/10/R78

  • G.G. Presting L. Malysheva J. Fuchs I. Schubert (1998) ArticleTitleA Ty3/Gypsy retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes Plant J. 16 721–728 Occurrence Handle10.1046/j.1365-313x.1998.00341.x Occurrence Handle10069078 Occurrence Handle1:CAS:528:DyaK1MXotlKmtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • C.D. Ryder L.B. Smith G.R. Teakle G.J. King (2001) ArticleTitleContrasting genome organisation: two regions of the Brassica oleracea genome compared with collinear regions of the Arabidopsis thaliana genome Genome 44 808–817 Occurrence Handle10.1139/gen-44-5-808 Occurrence Handle11681604 Occurrence Handle1:CAS:528:DC%2BD3MXos12lsrY%3D

    Article  PubMed  CAS  Google Scholar 

  • P. SanMiguel A. Tikhonov Y.K. Jin N. Motchoulskaia D. Zakharov A. Melake-Berhan P.S. Springer K.J. Edwards M. Lee Z. Avramova J.L. Bennetzen (1996) ArticleTitleNested retrotransposons in the intergenic regions of the maize genome Science 274 765–768 Occurrence Handle10.1126/science.274.5288.765 Occurrence Handle8864112 Occurrence Handle1:CAS:528:DyaK28XmsFOhsLs%3D

    Article  PubMed  CAS  Google Scholar 

  • P. SanMiguel B.S. Gaut A. Tikhonov Y. Nakajima J.L. Bennetzen (1998) ArticleTitleThe paleontology of intergene retrotransposons of maize Nature Genet. 20 43–45 Occurrence Handle9731528 Occurrence Handle1:CAS:528:DyaK1cXmtVOmtL4%3D

    PubMed  CAS  Google Scholar 

  • T. Schmidt (1999) ArticleTitleLINEs, SINEs and repetitive DNA: non-LTR retrotransposons in plant genomes Plant Mol. Biol. 40 903–910 Occurrence Handle10.1023/A:1006212929794 Occurrence Handle10527415 Occurrence Handle1:CAS:528:DyaK1MXmslGkurc%3D

    Article  PubMed  CAS  Google Scholar 

  • T. Schwarzacher J.S.(P.) Heslop-Harrison (2000) Practical In Situ Hybridization BIOS Scientific Publishers Ltd Oxford, UK

    Google Scholar 

  • C. Simillion K. Vandepoele M.C.E. Montagu ParticleVan M. Zabeau Y. Peer ParticleVan de (2002) ArticleTitleThe hidden duplication past of Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 99 13627–13632 Occurrence Handle10.1073/pnas.212522399 Occurrence Handle12374856 Occurrence Handle1:CAS:528:DC%2BD38XotVKmsbY%3D

    Article  PubMed  CAS  Google Scholar 

  • J. Terol M.C. Castillo M. Pérez-Alonso R. Frutos Particlede (2001) ArticleTitleStructural and evolutionary analysis of the copia-like elements in the Arabidopsis thaliana genome Mol. Biol. Evol. 18 882–892 Occurrence Handle11319272 Occurrence Handle1:CAS:528:DC%2BD3MXjtFykt7c%3D

    PubMed  CAS  Google Scholar 

  • InstitutionalAuthorNameU, N. (1935) ArticleTitleGenomic analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilisation Jpn. J. Bot. 7 389–452

    Google Scholar 

  • A.V. Vershinin A. Druka A.G. Alkhimova A. Kleinhofs J.S. Heslop-Harrison (2002) ArticleTitleLINEs and gypsy-like retrotransposons in Hordeum species Plant Mol. Biol. 49 1–14 Occurrence Handle10.1023/A:1014469830680 Occurrence Handle12008894 Occurrence Handle1:CAS:528:DC%2BD38XjtlemtL0%3D

    Article  PubMed  CAS  Google Scholar 

  • T.J. Vision D.G. Brown S.D. Tanksley (2000) ArticleTitleThe origins of genome duplications in Arabidopsis Science 290 2114–2117 Occurrence Handle10.1126/science.290.5499.2114 Occurrence Handle11118139 Occurrence Handle1:CAS:528:DC%2BD3cXptVyisr0%3D

    Article  PubMed  CAS  Google Scholar 

  • V. Walbot D.A. Petrov (2001) ArticleTitleGene galaxies in the maize genome Proc. Natl. Acad. Sci. USA 98 8163–8164 Occurrence Handle10.1073/pnas.161278798 Occurrence Handle11459945 Occurrence Handle1:CAS:528:DC%2BD3MXls1Wjtbk%3D

    Article  PubMed  CAS  Google Scholar 

  • Warwick, S.I., Francis, A., La Fleche, J., 2003. Guide to Wild Germplasm of Brassica and Allied Crops (tribe Brassiceae, Brassicaceae) 2nd Edition. http://www.brassica.info/crucifer%20genetics/brass00.pdf

  • Y. Xiong T.H. Eickbush (1990) ArticleTitleOrigin and evolution of retroelements based upon their reverse transcriptase sequences EMBO J. 9 3353–3362 Occurrence Handle1698615 Occurrence Handle1:CAS:528:DyaK3cXmt1Ghsbk%3D

    PubMed  CAS  Google Scholar 

  • Q. Zhang J. Arbuckle S.R. Wessler (2000) ArticleTitleRecent, extensive, and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker into genic regions of maize Proc. Natl. Acad. Sci. USA 97 1160–1165 Occurrence Handle10655501 Occurrence Handle1:CAS:528:DC%2BD3cXpvFemsA%3D%3D

    PubMed  CAS  Google Scholar 

  • X. Zhang S.R. Wessler (2004) ArticleTitleGenome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea Proc. Natl. Acad. Sci. USA 101 5589–5594 Occurrence Handle15064405 Occurrence Handle1:CAS:528:DC%2BD2cXjsVagu7k%3D

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Leicester, LE1 7RH, Leicester, UK

    Karine Alix & J. S. (Pat) Heslop-Harrison

  2. UMR de Génétique Végétale INRA/UPS/CNRS/INA P-G, Ferme du Moulon, 91190, Gif sur Yvette, France

    Karine Alix

  3. Warwick HRI, Wellesbourne, CV35 9EF, Warwick, UK

    Carol D. Ryder & Jay Moore

  4. Rothamsted Research, Harpenden, AL5 2QJ, Hertfordshire, UK

    Graham J. King

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  1. Karine Alix
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Alix, K., Ryder, C.D., Moore, J. et al. The Genomic Organization of Retrotransposons in Brassica oleracea. Plant Mol Biol 59, 839–851 (2005). https://doi.org/10.1007/s11103-005-1510-1

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