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A transcriptionally active copia-like retroelement in Citrus limon

Abstract

The plant nuclear genome is largely composed of mobile DNA, which can rearrange genomes and other individual gene structure and also affect gene regulation through various promoted activities: transposition, insertion, excision, chromosome breakage, and ectopic recombination. Ty1-copia-like retrotransposon is a widespread class of transposable elements in the plant kingdom, representing a large part of the total DNA content. Here, a novel retrotransposon-like sequence was isolated and identified as the Ty1-copia-like reverse transcriptase domain (named here CLCoy1), based on the homology of known elements. Fluorescence in situ hybridization, revealed that CLCoy1 was mainly located in telomeric and sub-telomeric regions along the Citrus chromosomes. CLCoy1 composes 3.6% of the genome and, interestingly, while transposons are mostly specific to a species, this element was identified in other Citrus species such as Citrus aurantium, Fortunella margarita and Citrus paradisi, but undetected in Poncirus trifoliata. We also determined that wounding, salt and cell culture stress produced transcriptional activation of this novel retroelement in Citrus limon. The novel Ty1-copia-like element CLCoy1 may have played a major role in shaping genome structure and size during Citrus species evolution.

Abbreviations

C. limon :

Citrus limon

PCR:

polymerase chain reaction

RT:

reverse transcriptase

References

  1. Kumar, A. and Bennetzen, J.L. Plant retrotransposons. Annu. Rev. Genet. 33 (1999) 479–532.

    Article  PubMed  CAS  Google Scholar 

  2. Lonnig, W.E. and Saedler, H. Plant transposons: contributors to evolution? Gene 205 (1997) 245–253.

    Article  PubMed  CAS  Google Scholar 

  3. Heslop-Harrison, J.S., Brandes, A., Taketa, S., Schmidt, T., Vershinin, A.V., Alkhimova, E.G., Kamm, A., Doudrick, R.L., Schwarzacher, T., Katsiotis, A., Kubis, S., Kumar, A., Pearce, S.R., Flavell, A.J. and Harrison, G.E. The chromosomal distribution of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution, Genetica 100 (1997) 197–204.

    Article  PubMed  CAS  Google Scholar 

  4. Bennetzen, J.L. Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 42 (2000) 251–269.

    Article  PubMed  CAS  Google Scholar 

  5. Su, P.Y. and Brown, T.A. Ty3/gypsy-like retrotransposon sequences in tomato. Plasmid 38 (1997) 148–157.

    Article  PubMed  CAS  Google Scholar 

  6. Voytas, D.F., Cummings, M.P., Konieczny, A., Ausubel, F.M. and Rodermel, S. Copia-like retrotransposons are ubiquitous among plants. Proc. Natl. Acad. Sci. USA 89 (1992) 7124–7128.

    Article  PubMed  CAS  Google Scholar 

  7. Grandbastien, M.A. Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3 (1998) 181–187.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  10. Fann, J.Y., Kovarik, A., Hemleben, V., Tsirekidze, N.I. and Beridze, T.G. Molecular and structural evolution of Citrus satellite DNA. Theor. Appl. Genet. 103 (2001) 1068–1073.

    Article  CAS  Google Scholar 

  11. Beridze, T., Tsirekidze, N. and Turishcheva, M.S. On the tertiary structure of the Citrus ichangensis satellite DNA. FEBS Lett. 338 (1994) 179–182.

    Article  PubMed  CAS  Google Scholar 

  12. Asins, M.J., Monforte, A.J., Mestre, P.F. and Carbonell, E.A. Citrus and Prunus copia-like retrotransposons. Theor. Appl. Genet. 99 (1999) 503–510.

    Article  CAS  Google Scholar 

  13. De Felice, B., Ciarmiello, L.F., Wilson, R.R. and Conicella, C. Molecular analysis of a novel tandemly organized repetitive DNA sequence in Citrus limon (L.) Burm. J. Appl. Genet. 48 (2007) 233–239.

    PubMed  Google Scholar 

  14. De Felice, B., Wilson, R.R., Ciarmiello, L.F., Scarano, M.T. and Ferrante, S. Characterization of a novel satellite DNA sequence from Flying Dragon (Poncirus trifoliata). Genetica 127 (2006) 45–53.

    Article  PubMed  CAS  Google Scholar 

  15. Wright, D.A., Ke, N., Smalle, J., Hauge, B.M., Goodman, H.M. and Voytas, D.F. Multiple non-LTR retrotransposons in the genome of Arabidopsis thaliana. Genetics 142 (1996) 569–578.

    PubMed  CAS  Google Scholar 

  16. Flavell, A.J., Smith, D.B. and Kumar, A. Extreme heterogeneity of Ty1-Copia group retrotransposons in plants. Mol. Genet. Genomics 231 (1992) 233–242.

    CAS  Google Scholar 

  17. Hirochika, H. and Hirochika, R. Ty1-copia group retrotransposons as ubiquitous components of plant genomes. J. Genet. 68 (1993) 35–46.

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  19. Friesen, N., Brandes, A. and Heslop-Harrison, J.S. Diversity, origin, and distribution of retrotransposons (gypsy and copia) in conifers. Mol. Biol. Evol. 18 (2001) 1176–1188.

    PubMed  CAS  Google Scholar 

  20. Murashige, T. and Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15 (1962) 473–497.

    Article  CAS  Google Scholar 

  21. Murray, M.G. and Thompson, W.F. Rapid isolation of high weight plant DNA. Nucleic Acids Res. 8 (1980) 4321–4325.

    Article  PubMed  CAS  Google Scholar 

  22. Thompson, J. D., Higgins, D.G. and Gibson, T.J. 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 (1994) 4673–4680.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  24. Tamura, K., Dudley, J., Nei, M. and Kumar, S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  25. Beguiristain, T., Grandbastien, M.A., Puigdomenech, P. and Casacuberta, J.M. Three Tnt1subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiol. 127 (2001) 212–221.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  27. Kalendar, R., Tanskanen, J., Immonen, S., Nevo, E. and Schulma, A.H. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc. Natl. Acad. Sci. USA 97 (2000) 6603–6607.

    Article  PubMed  CAS  Google Scholar 

  28. McClintock, B. The significance of responses of the genome to challenge. Science 226 (1984) 792–801.

    Article  PubMed  CAS  Google Scholar 

  29. Kidwell, M.G. and Lisch, D.R. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55 (2001) 1–24.

    PubMed  CAS  Google Scholar 

  30. Fedoroff, N. Transposons and genome evolution in plants. Proc. Natl. Acad. Sci. USA 97 (2000) 7002–7007.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  32. Miller, W.J., Hagemann, S., Reiter, E. and Pinsker, W. P-element homologous sequences are tandemly repeated in the genome of Drosophila guanche. Proc. Natl. Acad. Sci. USA 89 (1992) 4018–4022.

    Article  PubMed  CAS  Google Scholar 

  33. Volff, J.N. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28 (2006) 913–922.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Bruna De Felice.

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De Felice, B., Wilson, R.R., Argenziano, C. et al. A transcriptionally active copia-like retroelement in Citrus limon . Cell Mol Biol Lett 14, 289–304 (2009). https://doi.org/10.2478/s11658-008-0050-5

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