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The Ty1-copia families SALIRE and Cotzilla populating the Beta vulgaris genome show remarkable differences in abundance, chromosomal distribution, and age

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Abstract

Long terminal repeat (LTR) retrotransposons are major components of plant genomes influencing genome size and evolution. Using two separate approaches, we identified the Ty1-copia retrotransposon families Cotzilla and SALIRE in the Beta vulgaris (sugar beet) genome. While SALIRE elements are similar to typical Ty1-copia retrotransposons, Cotzilla elements belong to a lineage called Sireviruses. Hallmarks of Cotzilla retrotransposons are the existence of an additional putative env-like open reading frame upstream of the 3′LTR, an extended gag region, and a frameshift separating the gag and pol genes. Detected in a c 0 t-1 DNA library, Cotzilla elements belong to the most abundant retrotransposon families in B. vulgaris and are relatively homogenous and evolutionarily young. In contrast, the SALIRE family has relatively few copies, is diverged, and most likely ancient. As revealed by fluorescent in situ hybridization, SALIRE elements target predominantly gene-rich euchromatic regions, while Cotzilla retrotransposons are abundant in the intercalary and pericentromeric heterochromatin. The analysis of two retrotransposons from the same subclass contrasting in abundance, age, sequence diversity, and localization gives insight in the heterogeneity of LTR retrotransposons populating a plant genome.

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Abbreviations

BAC:

Bacterial artificial chromosome

DAPI:

4′,6′-diamidino-2-phenylindole

env :

Envelope

FISH:

Fluorescent in situ hybridization

FITC:

Fluorescein isothiocyanate

LTR:

Long terminal repeat

ORF:

Open reading frame

PBS:

Primer-binding site

PPT:

Polypurine tract

RT:

Reverse transcriptase

SDS:

Sodium dodecyl sulfate

SSC:

Standard saline citrate (1× SSC = 0.15 M NaCl, 0.015 M Na3-citrate)

TE:

Transposable element

References

  • Arumuganathan K, Earle E (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Report 9:208–218

    Article  CAS  Google Scholar 

  • Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36

    Article  CAS  PubMed  Google Scholar 

  • Birney E, Clamp M, Durbin R (2004) GeneWise and Genomewise. Genome Res 14:988–995

    Article  CAS  PubMed  Google Scholar 

  • Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–434

    Article  CAS  PubMed  Google Scholar 

  • Brandes A, Heslop-Harrison JS, Kamm A, Kubis S, Doudrick RL, Schmidt T (1997) Comparative analysis of the chromosomal and genomic organization of Ty1-copia-like retrotransposons in pteridophytes, gymnosperms and angiosperms. Plant Mol Biol 33:11–21

    Article  CAS  PubMed  Google Scholar 

  • Casacuberta J, Vernhettes S, Audeon C, Grandbastien MA (1997) Quasispecies in retrotransposons: a role for sequence variability in Tnt1 evolution. Genetica 100:109–117

    Article  CAS  PubMed  Google Scholar 

  • Dechyeva D, Gindullis F, Schmidt T (2003) Divergence of satellite DNA and interspersion of dispersed repeats in the genome of the wild beet Beta procumbens. Chromosome Res 11:3–21

    Article  CAS  PubMed  Google Scholar 

  • de Felice B, Wilson R, Argenziano C, Kafantaris I, Conicella C (2008) A transcriptionally active copia-like retroelement in Citrus limon. Cell Mol Biol Lett. doi:10.2478/s11658-008-0050-5

    PubMed  Google Scholar 

  • de Jong HJ, Fransz P, Zabel P (1999) High resolution FISH in plants—techniques and applications. Trends Plant Sci 4:258–263

    Article  Google Scholar 

  • Desel C, Jung C, Cai D, Kleine M, Schmidt T (2001) High-resolution mapping of YACs and the single-copy gene Hs1pro1 on Beta vulgaris chromosomes by multi-colour fluorescence in situ hybridization. Plant Mol Biol 45:113–122

    Article  CAS  PubMed  Google Scholar 

  • Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079

    Article  CAS  PubMed  Google Scholar 

  • Edgar R (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  PubMed  Google Scholar 

  • Francki MG (2001) Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.). Genome 44:266–274

    Article  CAS  PubMed  Google Scholar 

  • Gallo SA, Finnegan CM, Viard M et al (2003) The HIV Env-mediated fusion reaction. BBA - Biomembranes 1614:36–50

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Havecker ER, Baranov PV, Atkins JF, Voytas DF (2003) Translational recoding signals between gag and pol in diverse LTR retrotransposons. RNA 9:1422–1430

    Article  CAS  PubMed  Google Scholar 

  • Gindullis F, Dechyeva D, Schmidt T (2001a) Construction and characterization of a BAC library for the molecular dissection of a single wild beet centromere and sugar beet (Beta vulgaris) genome analysis. Genome 44:846–855

    Article  CAS  PubMed  Google Scholar 

  • Gindullis F, Desel C, Galasso I, Schmidt T (2001b) The large-scale organization of the centromeric region in Beta species. Genome Res 11:253–265

    Article  CAS  PubMed  Google Scholar 

  • Grandbastien MA, Audeon C, Casacuberta JM et al (1994) Functional analysis of the tobacco Tnt1 retrotransposon. Genetica 93:181–189

    Article  CAS  PubMed  Google Scholar 

  • Havecker ER, Gao X, Voytas DF (2005) The Sireviruses, a plant-specific lineage of the Ty1/copia retrotransposons, interact with a family of proteins related to dynein light chain 8. Plant Physiol 139:857–868

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison JS, Schwarzacher T, Anamthawat-Jónsson K, Leitch AR, Shi M, Leitch IJ (1991) In-situ hybridization with automated chromosome denaturation. Technique 3:109–116

    Google Scholar 

  • Heslop-Harrison JS, Brandes A, Taketa S et al (1997) The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100:197–204

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  Google Scholar 

  • Hirochika H, Fukuchi A, Kikuchi F (1992) Retrotransposon families in rice. Mol Gen Genet 233:209–216

    Article  CAS  PubMed  Google Scholar 

  • Hirochika H, Otsuki H, Yoshikawa M, Otsuki Y, Sugimoto K, Takeda S (1996) Autonomous transposition of the tobacco retrotransposon Tto1 in rice. Plant Cell 8:725–734

    Article  CAS  PubMed  Google Scholar 

  • Holligan D, Zhang X, Jiang N, Pritham EJ, Wessler SR (2006) The transposable element landscape of the model legume Lotus japonicus. Genetics 174:2215–2228

    Article  CAS  PubMed  Google Scholar 

  • Hull R (2001) Classifying reverse transcribing elements: a proposal and a challenge to the ICTV. Arch Virol 146:2255–2261

    Article  CAS  PubMed  Google Scholar 

  • Jia J, Yang Z, Li G, Liu C, Lei M, Zhang T, Zhou J, Ren Z (2009) Isolation and chromosomal distribution of a novel Ty1-copia-like sequence from Secale, which enables identification of wheat—Secale africanum introgression lines. J Appl Genet 50:25–28

    CAS  PubMed  Google Scholar 

  • Kapitonov V, Jurka J (1999) Molecular paleontology of transposable elements from Arabidopsis thaliana. Genetica 107:27–37

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Tosa Y, Shimada S, Sogo R, Kusaba M, Sunaga T, Betsuyaku S, Eto Y, Nakayashiki H, Mayama S (2001) OARE-1, a Ty1-copia retrotransposon in oat activated by abiotic and biotic stresses. Plant Cell Physiol 42:1345–1354

    Article  CAS  PubMed  Google Scholar 

  • Kloc A, Martienssen R (2008) RNAi, heterochromatin and the cell cycle. Trends Genet 24:511–517

    Article  CAS  PubMed  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    CAS  PubMed  Google Scholar 

  • Kubis S, Heslop-Harrison JS, Desel C, Schmidt T (1998) The genomic organization of non-LTR retrotransposons (LINEs) from three Beta species and five other angiosperms. Plant Mol Biol 36:821–831

    Article  CAS  PubMed  Google Scholar 

  • Kumar A (1998) The evolution of plant retroviruses: moving to green pastures. Trends Plant Sci 3:371–374

    Article  Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532

    Article  CAS  PubMed  Google Scholar 

  • Kuykendall D, Shao J, Trimmer K (2009) A nest of LTR retrotransposons adjacent the disease resistance-priming gene NPR1 in Beta vulgaris L. U.S. Hybrid H20. Int J Plant Genomics. doi:10.1155/2009/576742

    PubMed  Google Scholar 

  • Lange C, Holtgräwe D, Schulz B, Weisshaar B, Himmelbauer H (2008) Construction and characterization of a sugar beet (Beta vulgaris) fosmid library. Genome 51:948–951

    Article  CAS  PubMed  Google Scholar 

  • Laten HM, Majumdar A, Gaucher EA (1998) SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. Proc Natl Acad Sci USA 95:6897–6902

    Article  CAS  PubMed  Google Scholar 

  • Le Q, Melayah D, Bonnivard E, Petit M, Grandbastien MA (2007) Distribution dynamics of the Tnt1 retrotransposon in tobacco. Mol Genet Genomics 278:639–651

    Article  CAS  PubMed  Google Scholar 

  • Lerat E, Capy P (1999) Retrotransposons and retroviruses: analysis of the envelope gene. Mol Biol Evol 16:1198–1207

    CAS  PubMed  Google Scholar 

  • Lescot M, Dehais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  Google Scholar 

  • Lupas A (1996) Prediction and analysis of coiled-coil structures. Methods Enzymol 266:513–525

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869

    Article  CAS  PubMed  Google Scholar 

  • Malik HS, Henikoff S, Eickbush TH (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10:1307–1318

    Article  CAS  PubMed  Google Scholar 

  • McGrath JM, Shaw RS, de los Reyes BG, Weiland JJ (2004) Construction of a sugar beet BAC library from a hybrid with diverse traits. Plant Mol Biol Report 22:23–28

    Article  CAS  Google Scholar 

  • Menzel G, Dechyeva D, Wenke T, Holtgräwe D, Weisshaar B, Schmidt T (2008) Diversity of a complex centromeric satellite and molecular characterization of dispersed sequence families in sugar beet (Beta vulgaris). Ann Bot 102:521–530

    Article  CAS  PubMed  Google Scholar 

  • Miguel C, Simões M, Oliveira M, Rocheta M (2008) Envelope-like retrotransposons in the plant kingdom: evidence of their presence in gymnosperms (Pinus pinaster). J Mol Evol 67:517–525

    Article  CAS  PubMed  Google Scholar 

  • Moisy C, Garrison K, Meredith C, Pelsy F (2008) Characterization of ten novel Ty1/copia-like retrotransposon families of the grapevine genome. BMC Genomics 9:469

    Article  PubMed  Google Scholar 

  • Mroczek RJ, Dawe RK (2003) Distribution of retroelements in centromeres and neocentromeres of maize. Genetics 165:809–819

    CAS  PubMed  Google Scholar 

  • Nagaki K, Cheng Z, Ouyang S et al (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145

    Article  CAS  PubMed  Google Scholar 

  • Pagni M, Ioannidis V, Cerutti L, Zahn-Zabal M, Jongeneel CV, Falquet L (2004) MyHits: a new interactive resource for protein annotation and domain identification. Nucleic Acids Res 32:W332

    Article  CAS  PubMed  Google Scholar 

  • Pearce SR (2007) SIRE-1, a putative plant retrovirus is closely related to a legume Ty1-copia retrotransposon family. Cell Mol Biol Lett 12:120–126

    Article  CAS  PubMed  Google Scholar 

  • Pearce SR, Harrison G, Li D, Heslop-Harrison JS, Kumar A, Flavell AJ (1996) The Ty1-copia group retrotransposons in Vicia species: copy number, sequence heterogeneity and chromosomal localisation. Mol Gen Genet 250:305–315

    CAS  PubMed  Google Scholar 

  • Peterson-Burch BD, Voytas DF (2002) Genes of the Pseudoviridae (Ty1/copia retrotransposons). Mol Biol Evol 19:1832–1845

    CAS  PubMed  Google Scholar 

  • Peterson-Burch BD, Wright DA, Laten HM, Voytas DF (2000) Retroviruses in plants? Trends Genet 16:151–152

    Article  CAS  PubMed  Google Scholar 

  • Ramallo E, Kalendar R, Schulman A, Martínez-Izquierdo J (2008) Reme1, a copia retrotransposon in melon, is transcriptionally induced by UV light. Plant Mol Biol 66:137–150

    Article  CAS  PubMed  Google Scholar 

  • Rico-Cabanas L, Martínez-Izquierdo J (2007) CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis. Mol Genet Genomics 277:365–377

    Article  CAS  PubMed  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    Article  CAS  PubMed  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 

  • SanMiguel P, Tikhonov A, Jin YK (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768

    Article  CAS  PubMed  Google Scholar 

  • SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45

    Article  CAS  PubMed  Google Scholar 

  • Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends Plant Sci 3:195–199

    Article  Google Scholar 

  • Schmidt T, Jung C, Metzlaff M (1991) Distribution and evolution of two satellite DNAs in the genus Beta. Theor Appl Genet 82:793–799

    Article  CAS  Google Scholar 

  • Schmidt T, Schwarzacher T, Heslop-Harrison JS (1994) Physical mapping of rRNA genes by fluorescent in-situ hybridization and structural analysis of 5S rRNA genes and intergenic spacer sequences in sugar beet (Beta vulgaris). Theor Appl Genet 88:629–636

    Article  CAS  Google Scholar 

  • Schmidt T, Kubis S, Heslop-Harrison JS (1995) Analysis and chromosomal localization of retrotransposons in sugar beet (Beta vulgaris L.): LINEs and Ty1-copia-like elements as major components of the genome. Chromosome Res 3:335–345

    Article  CAS  PubMed  Google Scholar 

  • Shen Y, Ford-Lloyd BV, Newbury HJ (1998) Genetic relationships within the genus Beta determined using both PCR-based marker and DNA sequencing techniques. Heredity 80:624–632

    Article  CAS  PubMed  Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    Article  CAS  PubMed  Google Scholar 

  • Song SU, Gerasimova T, Kurkulos M, Boeke JD, Corces VG (1994) An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev 8:2046–2057

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Vershinin AV, Ellis THN (1999) Heterogeneity of the internal structure of PDR1, a family of Ty1/copia-like retrotransposons in pea. Mol Gen Genet 262:703–713

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Liu JS (2008) LTR retrotransposon landscape in Medicago truncatula: more rapid removal than in rice. BMC Genomics 9:382

    Article  PubMed  Google Scholar 

  • Weber B, Schmidt T (2009) Nested Ty3-gypsy retrotransposons of a single Beta procumbens centromere contain a putative chromodomain. Chromosome Res 17:379–396

    Article  CAS  PubMed  Google Scholar 

  • Wicker T, Keller B (2007) Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res 17:1072–1081

    Article  CAS  PubMed  Google Scholar 

  • Wright DA, Voytas DF (2002) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12:122–131

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Yamagata H, Hayashi-Tsugane M et al (2004) Composition and structure of the centromeric region of rice chromosome 8. Plant Cell 16:967–976

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

    CAS  PubMed  Google Scholar 

  • Zakrzewski F, Wenke T, Holtgräwe D, Weisshaar B, Schmidt, T (2009) Analysis of a c0t-1 library enables the targeted identification of minisatellite and satellite families in Beta vulgaris. BMC Plant Biol (in press)

  • Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Ines Walter for excellent technical assistance. Tony Heitkam acknowledges a fellowship and financial support of the FAZIT foundation. Torsten Wenke is funded by the BMBF grant “KMU-innovativ-2: Entwicklung von Retrotransposon-basierten molekularen Werkzeugen für die Züchtung, Sortenidentifizierung und Genbankerhaltung von Kartoffeln” (0315425B).

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  1. Department of Biology, Dresden University of Technology, 01069, Dresden, Germany

    Beatrice Weber, Torsten Wenke, Ulrike Frömmel, Thomas Schmidt & Tony Heitkam

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  1. Beatrice Weber
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  2. Torsten Wenke
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  3. Ulrike Frömmel
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Correspondence to Thomas Schmidt.

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Responsible Editor: JS (Pat) Heslop-Harrison.

Beatrice Weber and Torsten Wenke contributed equally to the manuscript.

Electronic Supplementary Materials

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S1

Schematic representation of an alignment containing the Cotzilla1 LTRs and 20 c 0 t-1 sequences similar to the Cotzilla1 LTR. Black bars represent sequences. The percentage identity relative to the Cotzilla1 5′LTR is indicated. These c 0 t-1 sequences were crucial for the identification of Cotzilla1. A BLAST search in the EMBL database using their consensus as query showed homology to BAC EF101866 containing the full-length retrotransposon Cotzilla1. (PDF 69 kb)

S2

Schematic representation of an alignment containing the complete Cotzilla1 retrotransposon and 347 homologous BAC sequences. Black bars represent sequences. Compared with Cotzilla1, the minimum sequence identity is 59%, the maximum sequence identity 99%. In average, the identity is 94% indicating that Cotzilla1 is a typical member of the Cotzilla family. Available BAC sequences have been generated by end-sequencing of HindIII cloned Beta vulgaris fragments (McGrath et al. 2004). Several regions of Cotzilla1 are underrepresented by BAC sequences since they do not contain HindIII restriction sites. (PDF 251 kb)

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Weber, B., Wenke, T., Frömmel, U. et al. The Ty1-copia families SALIRE and Cotzilla populating the Beta vulgaris genome show remarkable differences in abundance, chromosomal distribution, and age. Chromosome Res 18, 247–263 (2010). https://doi.org/10.1007/s10577-009-9104-4

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