Skip to main content
SpringerLink
Log in

FaRE1: a transcriptionally active Ty1-copia retrotransposon in strawberry

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Retrotransposons are ubiquitous in the plant kingdom and constitute a large fraction of many plant genomes. Although most retrotransposons from plants were thought to be transcriptionally silent in somatic tissues, evidence of activity under certain conditions is available in some cases. In this study, a complete LTR retrotransposon was isolated from the cultivated strawberry (Fragaria × ananassa) genome using genome walking. The element, named FaRE1, has all the features of a typical Ty1-copia retrotransposon. Its total length was 5,104 bp, comprising a single 3,891 bp open reading frame. It is represented by ~96 copies per genome, equivalent to ~0.33% of the genome. Transcription of FaRE1 was detected in leaf tissue treated with various phytohormones, such as naphthalene acetic acid, 2,4-dichlorophenoxyacetic acid or abscisic acid . To our knowledge, this is the first report of the isolation of a complete LTR retrotransposon with transcriptional activity in strawberry.

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

cDNA:

Complementary deoxyribonucleic acid

LTR:

Long terminal repeat

ORF:

Open reading frame

PCR:

Polymerase chain reaction

RT-PCR:

Reverse transcription polymerase chain reaction

TE:

Transposable element

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    Article  PubMed  CAS  Google Scholar 

  • Anaya N, Roncero MI (1995) Skippy, a retrotransposon from the fungal plant pathogen Fusarium oxysporum. Mol Gen Genet 249:637–647

    Article  PubMed  CAS  Google Scholar 

  • Baumann K, De Paolis A, Costantino P, Gualberti G (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11:323–334

    Article  PubMed  CAS  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 

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

    Article  PubMed  CAS  Google Scholar 

  • Boyle B, Brisson N (2001) Repression of the defense gene PR-10a by the single-stranded DNA binding protein SEBF. Plant Cell 13:2525–2537

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Zhang Z, Yang H, Li H, Dai H (2007) Detection of strawberry RNA and DNA viruses by RT-PCR using total nucleic acid as a template. J Phytopathol 155:431–436

    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 251:665–674

    PubMed  CAS  Google Scholar 

  • Flavell AJ, Pearce SR, Kumar A (1994) Plant transposable elements and the genome. Curr Opin Genet Dev 4:838–844

    Article  PubMed  CAS  Google Scholar 

  • Friesen PD, Nissen MS (1990) Gene organization and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome. Mol Cell Biol 10:3067–3077

    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 

  • Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573

    Article  PubMed  CAS  Google Scholar 

  • Gojobori T, Moriyama EN, Kimura M (1990) Molecular clock of viral evolution, and the neutral theory. Proc Natl Acad Sci USA 87:10015–10018

    Article  PubMed  CAS  Google Scholar 

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

    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 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  PubMed  CAS  Google Scholar 

  • Hansen LJ, Chalker DL, Sandmeyer SB (1988) Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol 8:5245–5256

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Kato H, Sriprasertsak P, Seki H, Ichinose Y, Shiraishi T, Yamada T (1999) Functional analysis of retrotransposons in pea. Plant Cell Physiol 40:933–941

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  PubMed  CAS  Google Scholar 

  • Liubomirskaia NV, Kim AI, IuV Il’in (2003) Retrotransposon MDG4 and its role in genetic instability of a mutator strain of Drosophila melanogaster. Genetika 39:164–172

    PubMed  CAS  Google Scholar 

  • Lonnig WE, Saedler H (2002) Chromosome rearrangements and transposable elements. Annu Rev Genet 36:389–410

    Article  PubMed  CAS  Google Scholar 

  • Ma Y (2008) Dissertation for doctorate: isolation and detection of LTR retrotransposon sequences from strawberry genome. Senyang Agricultural University, China

  • Ma Y, Sun H, Zhao G, Dai H, Gao X, Li H, Zhang Z (2008) Isolation and characterization of genomic retrotransposon sequences from octoploid strawberry (Fragaria × ananassa Duch.). Plant Cell Rep 27:499–507

    Article  PubMed  CAS  Google Scholar 

  • MacRae AF (1998) A pentamer-repeat-comtaining DNA sequence in Texas bluebonnet (Lupinus texensis Hook.). Genome 41:553–559

    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 

  • 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 

  • Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314

    Article  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 

  • Nehra NS, Kartha KK, Stushnoff C (1991) Nuclear DNA content and isozyme variation in relation to morphogenic potential of Strawberry (Fragaria × ananassa) callus cultures. Can J Bot 69:239–244

    Article  CAS  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:e258

    Article  PubMed  CAS  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 localization. Mol Gen Genet 250:305–315

    PubMed  CAS  Google Scholar 

  • Perlman PS, Boeke JD (2004) Molecular biology. Ring around the retroelement. Science 303:182–184

    Article  PubMed  CAS  Google Scholar 

  • Pontaroli AC, Rogers RL, Zhang Q, Shields ME, Davis TM, Folat KM, SanMiguel P, Bennetzen JL (2009) Gene content and distribution in the nuclear genome of Fragaria vesca. Plant Genome 2:93–101

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shim S, Lee SK, Han JK (2000) A novel family of retrotransposons in Xenopus with a developmentally regulated expression. Genesis 26:198–207

    Article  PubMed  CAS  Google Scholar 

  • Simovic N, Wolyn D, Jelenkovic G (1992) Sequence analysis of 18S ribosomal RNA gene in Fragaria × ananassa Duch. cultivated octoploid strawberry. Plant Mol Biol 18:1217–1220

    Article  PubMed  CAS  Google Scholar 

  • Sprinzl M, Steegborn C, Hübel F, Steinberg S (1996) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 24:68–72

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi A, Narvanto A, Schulman AH (1996) The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol Biol 31:365–376

    Article  Google Scholar 

  • Tahara M, Aoki T, Suzuka S, Yamashita H, Tanaka M, matsunaga S, Kokumai S (2004) Isolation of an active element from a high-copy-number family of retrotransposons in the sweetpotato genome. Mol Gen Genomics 272:116–127

    Article  CAS  Google Scholar 

  • Takeda S, Sugimoto K, Otsuki H, Hirochika H (1998) Transcriptional activation of the tobacco retrotransposon 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 retrotransposons Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J 18:383–393

    Article  PubMed  CAS  Google Scholar 

  • Tapia G, Verdugo I, Yañez 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 Lycopersicon chilense Dun. Plant Physiol 138:2075–2086

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H, Marion-Poll A, Meyer C, Faure JD, Marin E, Caboche M (1992) Interest in and limits to the utilization of reporter genes for the analysis of transcriptional regulation of nitrate reductase. Mol Gen Genet 235:259–268

    Article  PubMed  CAS  Google Scholar 

  • White SE, Habera LF, Wessler SR (1994) Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci USA 91:11792–11796

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by National Natural Science Foundation of China (Grant No. 30871689) and Program for New Century Excellent Talents in University (NCET-07-0565).

Author information

Authors and Affiliations

  1. College of Horticulture, Shenyang Agricultural University, Dongling Road 120, 110161, Shenyang, Liaoning, People’s Republic of China

    Ping He, Yue Ma, Guiling Zhao, Hongyan Dai, He Li, Linlin Chang & Zhihong Zhang

Authors
  1. Ping He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yue Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guiling Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongyan Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. He Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Linlin Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhihong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhihong Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

He, P., Ma, Y., Zhao, G. et al. FaRE1: a transcriptionally active Ty1-copia retrotransposon in strawberry. J Plant Res 123, 707–714 (2010). https://doi.org/10.1007/s10265-009-0290-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-009-0290-0

Keywords

Search

Navigation