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. 2008 Dec 24;14(2):289–304. doi: 10.2478/s11658-008-0050-5

A transcriptionally active copia-like retroelement in Citrus limon

Bruna De Felice 1,✉, Robert R Wilson 1, Carolina Argenziano 1, Ioanis Kafantaris 1, Clara Conicella 2
PMCID: PMC6275675  PMID: 19115051

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.

Key words: Ty1-copia-like, Citrus, Transcription, Biotic and abiotic stress

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Abbreviations used

C. limon

Citrus limon

PCR

polymerase chain reaction

RT

reverse transcriptase

References

  • 1.Kumar A., Bennetzen J.L. Plant retrotransposons. Annu. Rev. Genet. 1999;33:479–532. doi: 10.1146/annurev.genet.33.1.479. [DOI] [PubMed] [Google Scholar]
  • 2.Lonnig W.E., Saedler H. Plant transposons: contributors to evolution? Gene. 1997;205:245–253. doi: 10.1016/S0378-1119(97)00397-1. [DOI] [PubMed] [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., Harrison G.E. The chromosomal distribution of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica. 1997;100:197–204. doi: 10.1023/A:1018337831039. [DOI] [PubMed] [Google Scholar]
  • 4.Bennetzen J.L. Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 2000;42:251–269. doi: 10.1023/A:1006344508454. [DOI] [PubMed] [Google Scholar]
  • 5.Su P.Y., Brown T.A. Ty3/gypsy-like retrotransposon sequences in tomato. Plasmid. 1997;38:148–157. doi: 10.1006/plas.1997.1310. [DOI] [PubMed] [Google Scholar]
  • 6.Voytas D.F., Cummings M.P., Konieczny A., Ausubel F.M., Rodermel S. Copia-like retrotransposons are ubiquitous among plants. Proc. Natl. Acad. Sci. USA. 1992;89:7124–7128. doi: 10.1073/pnas.89.15.7124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Grandbastien M.A. Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 1998;3:181–187. doi: 10.1016/S1360-1385(98)01232-1. [DOI] [Google Scholar]
  • 8.Hirochika H., Sugimoto K., Otsuki Y., Kanda M. Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci. USA. 1996;93:7783–7788. doi: 10.1073/pnas.93.15.7783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Hirochika H. Activation of tobacco retrotransposons during tissue culture. EMBO J. 1993;12:2521–2528. doi: 10.1002/j.1460-2075.1993.tb05907.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Fann J.Y., Kovarik A., Hemleben V., Tsirekidze N.I., Beridze T.G. Molecular and structural evolution of Citrus satellite DNA. Theor. Appl. Genet. 2001;103:1068–1073. doi: 10.1007/s001220100719. [DOI] [Google Scholar]
  • 11.Beridze T., Tsirekidze N., Turishcheva M.S. On the tertiary structure of the Citrus ichangensis satellite DNA. FEBS Lett. 1994;338:179–182. doi: 10.1016/0014-5793(94)80360-9. [DOI] [PubMed] [Google Scholar]
  • 12.Asins M.J., Monforte A.J., Mestre P.F., Carbonell E.A. Citrus and Prunus copia-like retrotransposons. Theor. Appl. Genet. 1999;99:503–510. doi: 10.1007/s001220051263. [DOI] [PubMed] [Google Scholar]
  • 13.De Felice B., Ciarmiello L.F., Wilson R.R., Conicella C. Molecular analysis of a novel tandemly organized repetitive DNA sequence in Citrus limon (L.) Burm. J. Appl. Genet. 2007;48:233–239. doi: 10.1007/BF03195217. [DOI] [PubMed] [Google Scholar]
  • 14.De Felice B., Wilson R.R., Ciarmiello L.F., Scarano M.T., Ferrante S. Characterization of a novel satellite DNA sequence from Flying Dragon (Poncirus trifoliata) Genetica. 2006;127:45–53. doi: 10.1007/s10709-005-2479-z. [DOI] [PubMed] [Google Scholar]
  • 15.Wright D.A., Ke N., Smalle J., Hauge B.M., Goodman H.M., Voytas D.F. Multiple non-LTR retrotransposons in the genome of Arabidopsis thaliana. Genetics. 1996;142:569–578. doi: 10.1093/genetics/142.2.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Flavell A.J., Smith D.B., Kumar A. Extreme heterogeneity of Ty1-Copia group retrotransposons in plants. Mol. Genet. Genomics. 1992;231:233–242. doi: 10.1007/BF00279796. [DOI] [PubMed] [Google Scholar]
  • 17.Hirochika H., Hirochika R. Ty1-copia group retrotransposons as ubiquitous components of plant genomes. J. Genet. 1993;68:35–46. doi: 10.1266/jjg.68.35. [DOI] [PubMed] [Google Scholar]
  • 18.Suoniemi A., Tanskanen J., Schulman A.H. Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J. 1998;13:699–705. doi: 10.1046/j.1365-313X.1998.00071.x. [DOI] [PubMed] [Google Scholar]
  • 19.Friesen N., Brandes A., Heslop-Harrison J.S. Diversity, origin, and distribution of retrotransposons (gypsy and copia) in conifers. Mol. Biol. Evol. 2001;18:1176–1188. doi: 10.1093/oxfordjournals.molbev.a003905. [DOI] [PubMed] [Google Scholar]
  • 20.Murashige T., Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 1962;15:473–497. doi: 10.1111/j.1399-3054.1962.tb08052.x. [DOI] [Google Scholar]
  • 21.Murray M.G., Thompson W.F. Rapid isolation of high weight plant DNA. Nucleic Acids Res. 1980;8:4321–4325. doi: 10.1093/nar/8.19.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Thompson J. D., Higgins D.G., 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. 1994;22:4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987;4:406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  • 24.Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007;24:1596–1599. doi: 10.1093/molbev/msm092. [DOI] [PubMed] [Google Scholar]
  • 25.Beguiristain T., Grandbastien M.A., Puigdomenech P., Casacuberta J.M. Three Tnt1subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiol. 2001;127:212–221. doi: 10.1104/pp.127.1.212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Kimura Y., Tosa Y., Shimada S., Sogo S., Kusaba M., Sunaga T., Betsuyaku S., Eto Y., Nakayashiki H., Mayama S. OARE-1, a Ty1- copia retrotransposon in oat activated by abiotic and biotic stresses. Plant Cell Physiol. 2001;42:1345–1354. doi: 10.1093/pcp/pce171. [DOI] [PubMed] [Google Scholar]
  • 27.Kalendar R., Tanskanen J., Immonen S., Nevo E., 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. 2000;97:6603–6607. doi: 10.1073/pnas.110587497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.McClintock B. The significance of responses of the genome to challenge. Science. 1984;226:792–801. doi: 10.1126/science.15739260. [DOI] [PubMed] [Google Scholar]
  • 29.Kidwell M.G., Lisch D.R. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution. 2001;55:1–24. doi: 10.1111/j.0014-3820.2001.tb01268.x. [DOI] [PubMed] [Google Scholar]
  • 30.Fedoroff N. Transposons and genome evolution in plants. Proc. Natl. Acad. Sci. USA. 2000;97:7002–7007. doi: 10.1073/pnas.97.13.7002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Rico-Cabanas L., Martinez-Izquierdo J.A. CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis. Mol. Genet. Genomics. 2007;277:365–377. doi: 10.1007/s00438-006-0200-2. [DOI] [PubMed] [Google Scholar]
  • 32.Miller W.J., Hagemann S., Reiter E., Pinsker W. P-element homologous sequences are tandemly repeated in the genome of Drosophila guanche. Proc. Natl. Acad. Sci. USA. 1992;89:4018–4022. doi: 10.1073/pnas.89.9.4018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Volff J.N. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays. 2006;28:913–922. doi: 10.1002/bies.20452. [DOI] [PubMed] [Google Scholar]

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