Skip to main content
SpringerLink
Log in

CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

LTR retrotransposons (LTR-RTNs) are widespread constituents of eukaryote genomes, particularly plant genomes. Although LTR-RTNs from plants were thought to be transcriptionally silent in somatic tissues, evidences of activity under certain conditions are available for some of them. In order to investigate LTR-RTNs in the Citrus sinensis genome, we analysed them by PCR using degenerate primers corresponding to highly conserved domains. All elements of the two types of LTR-RTN comprise about 23% of the genome, the copia group contribution being higher (13%) than the gypsy one (10%). From dendogram analysis, we report seven new copia RTN families, named CIRE1 to CIRE7. Here, we report on the first complete retrotransposon identified in Citrus (named CIRE1), which has all the features of a typical copia RTN. CIRE1 retrotransposon has around 2,200 full-length copies, contributing to 2.9% of the C. sinensis genome. CIRE1 has a root-specific expression in sweet orange plants. We have also determined that wounding and exogenous application of plant hormones, as methyl jasmonate and auxin, increase the transcription level of CIRE1 in leaf tissues. In addition, we show that CIRE1 5′LTR promoter can drive transient expression of the gus reporter gene in heterologous plant systems. These findings confirm CIRE1 as one of the few transcriptionally active RTNs described in plants and to our knowledge the first one to be reported in Citrus species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

EST:

Expressed sequence tag

GUS:

β-glucuronidase

LTR:

Long terminal repeat

MeJA:

Methyl jasmonate

NAA:

Naphthaleneacetic acid

ON:

Overnight

ORF:

Open reading frame

PCR:

Polymerase chain reaction

RT:

Reverse transcriptase

RTN:

Retrotransposon

TE:

Transposable element

References

  • Aledo R, Raz R, Monfort A, Vicient CM, Puigdomènech P, Martínez-Izquierdo JA (1995) Chromosome localization and characterization of a family of long interspersed repetitive DNA elements from the genus Zea. Theor Appl Genet 90:1094–1100

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403

    PubMed  CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the florewing plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Araujo PG, Casacuberta JM, Costa APP, Hashimoto RY, Grandbastien MA, Van Sluys MA (2001) Retrolyc1 subfamilies defined by different U3 LTR regulatory regions in the Lycopersicon genus. Mol Genet Genomics 266:35–41

    Article  PubMed  CAS  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA Content of Some Important Plant Species. Plant Mol Biol Rep 9:211–215

    Google Scholar 

  • Asíns M, Monforte A, Mestre P, Carbonell E (1999) Citrus and Prunus copia-like retrotransposons. Theor Appl Genet 99:503–510

    Article  Google Scholar 

  • Beguiristain T, Grandbastien MA, Puigdomenech P, Casacuberta JM (2001) Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiol 127:212–221

    Article  PubMed  CAS  Google Scholar 

  • Bernet GP, Asins MJ (2003) Identification and genomic distribution of gypsy like retrotransposons in Citrus and Poncirus. Theor Appl Genet 108(1):121–130

    Article  PubMed  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Bretó MO, Ruiz C, Pina JA, Asins MJ (2001) The diversification of Citrus clementina Hort. Ex Tan., a vegetatively propagated crop species. Mol Phylogenet Evol 21:285–293

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Costa AP, Scortecci KC, Hashimoto RY, Araujo PG, Grandbastien MA, Van Sluys MA (1999) Retrolyc1–1, a member of the Tntl retrotransposon super-family in the Lycopersicon peruvianum genome. Genetica 107:65–72

    Article  CAS  Google Scholar 

  • Farman ML, Tosa Y, Nitta N, Leong SA (1996) MAGGY, a retrotransposon in the genome of the rice blast fungus Magnaporthe grisea. Mol Gen Genet 251(6):665–674

    PubMed  CAS  Google Scholar 

  • Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134

    Article  PubMed  CAS  Google Scholar 

  • Feng DF, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25:351–360

    PubMed  CAS  Google Scholar 

  • Flavell AJ, Smith DB, Kumar A (1992) Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol Gen Genet 231:233–242

    PubMed  CAS  Google Scholar 

  • García-Martínez J, Martínez-Izquierdo JA (2003) Study on the evolution of the Grande retrotransposon in the Zea genus. Mol Biol Evol 20:831–841

    Article  PubMed  CAS  Google Scholar 

  • Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3(5):181–187

    Article  Google Scholar 

  • Grandbastien MA, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380

    Article  PubMed  CAS  Google Scholar 

  • Grandbastien M, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa APP, Le QH, Melayah D, Petit M, Poncet C, Tam SM, Van Sluys MA, Mhiri C (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res 110:229–241

    Article  PubMed  CAS  Google Scholar 

  • Gribbon BM, Pearce SR, Kalendar R, Schulman AH, Paulin L, Jack P, Kumar A, Flavell AJ (1999) Phylogeny and transpositional activity of Ty1-copia group retrotransposons in cereal genomes. Mol Gen Genet 261:883–891

    Article  PubMed  CAS  Google Scholar 

  • Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inze D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351

    Article  PubMed  CAS  Google Scholar 

  • Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J. 12(6):2521–2528

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996b) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93:7783–7788

    Article  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Kentner EK, Arnold ML, Wessler SR (2003) Characterization of high-copy-number retrotransposons from the large genomes of the Lousiana Iris species and their use as molecular markers. Genetics 164:685–697

    PubMed  CAS  Google Scholar 

  • Kimura Y, Tosa Y, Shimada S, Sogo S, 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(12):1345–1354

    Article  PubMed  CAS  Google Scholar 

  • Konieczny A, Voytas DF, Cummings MP, Ausubel FM (1991) A superfamily of Arabidopsis thaliana retrotransposons. Genetics 127(4):801–809

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2.1: molecular evolutionary genetics analysis software, Bioinformatics 17:1244–1245

    Article  PubMed  CAS  Google Scholar 

  • Manninen I, Schulman AH (1993) BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.). Plant Mol Biol 22:829–846

    Article  PubMed  CAS  Google Scholar 

  • Marillonnet S, Wessler SR (1998) Extreme structural heterogeneity among the members of a maize retrotransposon family. Genetics 150:1245–1256

    PubMed  CAS  Google Scholar 

  • Marlor RL, Parkhurst SM, Corces VG (1986) The Drosophila melanogaster gypsy transposable elements encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 6:1129–1134

    PubMed  CAS  Google Scholar 

  • Melayah D, Bonnivard E, Chalhoub B, Audeon C, Grandbastien MA (2001) The mobility of the tobacco Tnt1 retrotransposon correlates with its transcriptional activation by fungal factors. Plant J 28(2):159–168

    Article  PubMed  CAS  Google Scholar 

  • Menossi M, Puigdomènech P, Martínez-Izquierdo JA (2000) Improved analysis of promoter activity in biolistically transformed plant cells. BioTechniques 28:54–58

    PubMed  CAS  Google Scholar 

  • Mount SM, Rubin GM (1985) Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol Cell Biol 5:1630–1638

    PubMed  CAS  Google Scholar 

  • Okamoto H, Hirochika H (2000) Efficient insertion mutagenesis of Arabidopsis by tissue culture-induced activation of the tobacco retrotransposon Tto1. Plant J 23(2):291–304

    Article  PubMed  CAS  Google Scholar 

  • Ollitrault P, Dambier D, Luro F, Duperray C (1995) Nuclear genome size variations in Citrus. Fruits 49:390–393

    Google Scholar 

  • Pearce SR, Harrison G, Li D, Heslop-Harrison J, 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

    PubMed  CAS  Google Scholar 

  • Pelissier T, Tutois S, Deragon J, Tourmente S, Genestier S, Picard G (1995) Athila, a new retroelement from Arabidopsis thaliana. Plant Mol Biol 29:441–452

    Article  PubMed  CAS  Google Scholar 

  • Pouteau S, Huttner E, Grandbastien MA, Caboche M (1991) Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J 10:1911–1918

    PubMed  CAS  Google Scholar 

  • Pouteau S, Grandbastien MA, Boccara M (1994) Microbial elicitors of plant defense responses activate transcription of a retrotransposon. Plant J 5(4):535–542

    CAS  Google Scholar 

  • Rozas J, Rozas R (1999) DnaSP version 3.14: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan D, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of maize genome. Science 274:765–768

    Article  PubMed  CAS  Google Scholar 

  • Sasaki T et al (2002) Genome sequence and structure of rice chromosome 1. Nature 420:312–316

    Article  PubMed  CAS  Google Scholar 

  • Smyth DR, Kalitsis P, Joseph JL, Sentry JW (1989) Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc Natl Acad Sci USA 86:5015–5019

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi A, Narvanto A, Schulman AH (1996) The BARE1 retrotransposon s transcribed in barley from a LTR promoter active in transient assays. Plant Mol Biol 31:365–376

    Article  Google Scholar 

  • Suoniemi A, Tanskanen J, Schulman AH (1998) Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J 13:699–705

    Article  PubMed  CAS  Google Scholar 

  • Takeda S, Sugimoto K, Otsuki H, Hirochika H (1998). Transcriptional activation of the tobacco retrotransposn Tto1 by wounding and methyl jasmonate. Plant Mol Biol 36:365–376

    Article  PubMed  CAS  Google Scholar 

  • Takeda S, Sugimoto K, Otsuki H, Hirochika H (1999) A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J 18(4):383–393

    Article  PubMed  CAS  Google Scholar 

  • Tapia G, Verdugo I, Yánez M, Ahumada I, Theoduloz C, Cordero C, Poblete F, González E, Ruiz-Lara S (2005) Involvement of ethylene in stress-induced expression of the TLC1–1 retrotransposon from Lycopersicum chilense Dun. Plant Physiol 138:2075–2086

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Turcich MP, Bokhari-Riza A, Hamilton DA, He C, Messier W, Stewart CB, Mascarenhas JP (1996) PREM-2, a copia-type retroelement in maize is expressed preferentially in early microspores. Sex Plant Reprod 9:65–74

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vicient CM (1995) Caracterización molecular de Grande1, un nuevo tipo de retrotransposón del género Zea. PhD Thesis, University of Barcelona, Spain

  • Vicient CM, Schulman AH (2002) Copia-like retrotransposons in the rice genome: few and assorted. Genome Lett 1:35–47

    Article  CAS  Google Scholar 

  • Vicient CM, Suoniemi A, Anamthawat-Jónsson K, Tanskanen J, Beharav A, Nevo E, Schulman AH (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11:1769–1784

    Article  PubMed  CAS  Google Scholar 

  • Vicient CM, Jääskeläinen MJ, Kalendar R, Schulman AH (2001) Active retrotransposons are a common feature of grass genomes. Plant Physiol 125:1283–1292

    Article  PubMed  CAS  Google Scholar 

  • Voytas DF, Cummings MP, Koniczny A, Ausubel FM, Rodermel SR (1992) Copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89:7124–7128

    Article  PubMed  CAS  Google Scholar 

  • Waugh R, McLean K, Flavell AJ, Pearce SR, Kumar A, Thomas BB, Powell W (1997) Genetic distribution of BARE-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol Gen Genet 253:687–694

    Article  PubMed  CAS  Google Scholar 

  • Wessler SR, Bureau TE, White SE (1995) LTR-retrotransposons and MITE: important players in the evolution of plant genomes. Curr Opin Genet Dev 5:814–821

    Article  PubMed  CAS  Google Scholar 

  • Yanez M, Verdugo I, Rodríguez M, Prats S, Ruiz-Lara S (1998) Highly heterogeneous families of Ty1/copia retrotransposons in the Lycopersicum chilense genome. Gene 222:223–228

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are indebted to Dr. Carlos Vicient and Dr. JM Casacuberta for critical reading of the manuscript. LRC was recipient of a predoctoral fellowships from Autonomous Catalan Government (Generalitat) (2001FI 00143). Some funds for this study were provided by CERBA (Generalitat of Catalonia). This work was mainly supported by the grant BIO99-1175 (CICYT) from the MEC of Spanish Govern to JAMI.

Author information

Authors and Affiliations

  1. Department of Molecular Genetics, Consorci CSIC-IRTA, C/Jordi Girona 18-26, 08034, Barcelona, Spain

    Laura Rico-Cabanas & José A. Martínez-Izquierdo

Authors
  1. Laura Rico-Cabanas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José A. Martínez-Izquierdo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Rico-Cabanas.

Additional information

Communicated by M.-A. Grandbastien.

Nucleotide sequence data reported are available in the EMBL database under the accession numbers AM117724 to AM117738, AM236246 to AM236248 (sweet orange copia-like rt sequences; CoSi1 to CoSi19) and AM040263 (CIRE1 retrotransposon).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rico-Cabanas, L., Martínez-Izquierdo, J.A. CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis . Mol Genet Genomics 277, 365–377 (2007). https://doi.org/10.1007/s00438-006-0200-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-006-0200-2

Keywords

Search

Navigation