Skip to main content
SpringerLink
Log in

CARE1, a TY3-gypsy like LTR-retrotransposon in the food legume chickpea (Cicer arietinum L.)

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

We report a Ty3-gypsy like retrotransposon CARE1 (Cicer arietinum retro-element 1) in chickpea (Accession no. DQ239702). This 5,920-bp AT-rich (63%) element carries 723-bp 5′-LTR and 897-bp 3′-LTR flanking to an internal region of 4,300-bp. The LTRs of CARE1 show 93.9% nucleotide identity to each other and have 4-bp (ACTA) terminal inverted repeats. A 17-bp potential tRNAmet primer binding site downstream to 5′-LTR and a 13-bp polypurine tract upstream to 3′-LTR have been identified. The order of characteristic domains (Gag-proteinase-reverse transcriptase-RNaseH-integrase) in the deduced amino acid sequence and its phylogenetic analysis with other retrotransposons, places CARE1 in the gypsy group of retrotransposons. Homologues of a number of cis-elements including CCAAT, TATA and GT-1 have been detected in the regulatory region or the 5′-LTR of CARE1. Transgenic tobacco plants containing 5′-LTR:GUS construct showed that its 5′-LTR is inactive in a heterologous system under normal as well as tissue culture conditions. Genomic Southern blot experiments using 5′-LTR of the element as a probe showed that CARE1 or its related elements are present in the genomes of various chickpea accessions from various geographic regions.

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

Similar content being viewed by others

Abbreviations

CARE1:

Cicer arietinum retro-element1

GUS:

β-glucuronidase gene

LTR:

Long terminal repeat

ORF:

Open reading frame

RT:

Reverse transcriptase

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389

    Article  PubMed  CAS  Google Scholar 

  • Ausubel MF, Brent R, Kungston R, Moore D, Seidman J, Smith J, Struhl K (1994) Current Protocols in Molecular Biology. Wiley, New York, pp 2.3.3–2.3.5

  • Benko-Iseppon AM, Winter P, Huettel B, Staginnus C, Muehlbauer FJ, Kahl G (2003) Molecular markers closely linked to fusarium resistance genes in chickpea show significant alignments to pathogenesis-related genes located on Arabidopsis chromosomes 1 and 5. Theor Appl Genet 107:379–386. doi:10.1007/s00122-003-1260-x

    Article  PubMed  CAS  Google Scholar 

  • Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond B Biol Sci 274:227–274. doi:10.1098/rstb.1976.0044

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269. doi:10.1023/A:1006344508454

    Article  PubMed  CAS  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. doi:10.1023/A:1005797222148

    Article  PubMed  CAS  Google Scholar 

  • Chavanne F, Zhang D, Liaud M, Cerff R (1998) Structure and evolution of Cyclops: a novel giant retrotransposon of the Ty3/Gypsy family highly amplified in pea and other legume species. Plant Mol Biol 37:363–375. doi:10.1023/A:1005969626142

    Article  PubMed  CAS  Google Scholar 

  • Doolittle RF, Feng DF, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Q Rev Biol 64:1–30. doi:10.1086/416128

    Article  PubMed  CAS  Google Scholar 

  • Dooner HK, He L (2008) Maize genome structure variation: interplay between retrotransposon polymorphisms and genic recombination. Plant Cell 20:249–258. doi:10.1105/tpc.107.057596

    Article  PubMed  CAS  Google Scholar 

  • Farabaugh PJ, Zhao H, Vimaladithan A (1993) A novel programed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast: frameshifting without tRNA slippage. Cell 74:93–103. doi:10.1016/0092-8674(93)90297-4

    Article  PubMed  CAS  Google Scholar 

  • Feng DF, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic tree. J Mol Evol 25:351–360. doi:10.1007/BF02603120

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341. doi:10.1038/nrg793

    Article  PubMed  CAS  Google Scholar 

  • Flavell AJ, Pearce SR, Kumar A (1994) Plant transposable elements and the genome. Curr Opin Genet Dev 4:838–844. doi:10.1016/0959-437X(94)90068-X

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto R, Takuno S, Sasaki T, Nishio T (2008) The pattern of amplification and differentiation of Ty1-copia and Ty3-gypsy retrotransposons in Brassicaceae species. Genes Genet Syst 83:13–22. doi:10.1266/ggs.83.13

    Article  PubMed  CAS  Google Scholar 

  • Grandbastien MA, Audeon C, Casacuberta JM, Grappin P, Lucas H, Moreau C, Pouteau S (1994) Functional analysis of the tobacco Tnt1 retrotransposon. Genetica 93:181–189. doi:10.1007/BF01435250

    Article  PubMed  CAS  Google Scholar 

  • Grandgenett DP, Mumm SR (1990) Unraveling retrovirus integration. Cell 60:3–4. doi:10.1016/0092-8674(90)90707-L

    Article  PubMed  CAS  Google Scholar 

  • Hawkins JS, Hu G, Rapp RA, Grafenberg JL, Wendel JF (2008) Phylogenetic determination of the pace of transposable element proliferation in plants: copia and LINE-like elements in Gossypium. Genome 51:8–11. doi:10.1139/G07-099

    Article  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. doi:10.1093/nar/27.1.297

    Article  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 

  • Horsch RB, Rogers SG, Fraley RT (1985) Transgenic plants. Cold Spring Harb Symp Quant Biol 50:433–437

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532. doi:10.1146/annurev.genet.33.1.479

    Article  PubMed  CAS  Google Scholar 

  • Kumekawa N, Ohtsubo H, Horiuchi T, Ohtsubo E (1999) Identification and characterization of novel retrotransposons of the gypsy type in rice. Mol Gen Genet 260:593–602. doi:10.1007/s004380050933

    Article  PubMed  CAS  Google Scholar 

  • Lall IP, Maneesha, Upadhyaya KC (2002) Panzee, a copia-like retrotransposon from the grain legume, pigeonpea (Cajanus cajan L.). Mol Genet Genomics 267:271–280. doi:10.1007/s00438-002-0674-5

    Article  PubMed  CAS  Google Scholar 

  • Lucas H, Feuerbach F, Kunert K, Grandbastein MA, Caboche M (1995) RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana. EMBO J 14:2364–2373

    PubMed  CAS  Google Scholar 

  • Madsen LH, Fukai E, Radutoiu S, Yost CK, Sandal N, Schauser L, Stougaard J (2005) LORE1, an active low-copy number Ty3-gypsy retrotransposon family in the model legume Lotus japonicus. Plant J 44:372–381. doi:10.1111/j.1365-313X.2005.02534.x

    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. doi:10.1007/BF00027369

    Article  PubMed  CAS  Google Scholar 

  • McClure MA (1991) Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol Biol Evol 8:835–856

    PubMed  CAS  Google Scholar 

  • Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KF, Wing RA (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354. doi:10.1073/pnas.0406163101

    Article  PubMed  CAS  Google Scholar 

  • Mhiri C, Morel JB, Vernhettes S, Casacuberta JM, Lucas M, Grandbastien MA (1997) The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol 33:257–266. doi:10.1023/A:1005727132202

    Article  PubMed  CAS  Google Scholar 

  • Muthukumar B, Bennetzen JL (2004) Isolation and characterization of genomic and transcribed retrotransposon sequences from sorghum. Mol Genet Genomics 271:308–316. doi:10.1007/s00438-004-0980-1

    Article  PubMed  CAS  Google Scholar 

  • Neumann P, Pozarkova D, Macas J (2003) Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced. Plant Mol Biol 53:399–410. doi:10.1023/B:PLAN.0000006945.77043.ce

    Article  PubMed  CAS  Google Scholar 

  • Nisole S, Saib A (2004) Early steps of retrovirus replicative cycle. Retrovirology 1:1–9. doi:10.1186/1742-4690-1-9

    Article  Google Scholar 

  • Pelissier T, Tutois S, Tourmente S, Deragon JM, Picard G (1996) DNA regions flanking the major Arabidopsis thaliana satellite are principally enriched in Athila retroelement sequences. Genetica 97:141–151. doi:10.1007/BF00054621

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD, Wessler SR (1994) Molecular evolution of Magellan, a maize Ty3/gypsy like retrotransposon. Proc Natl Acad Sci USA 91:11674–11678. doi:10.1073/pnas.91.24.11674

    Article  PubMed  CAS  Google Scholar 

  • Quinn JM, Merchant S (1995) Two copper-responsive elements associated with the Chlamydomonas Cyc6 gene function as targets for transcriptional activators. Plant Cell 7:623–628

    Article  PubMed  CAS  Google Scholar 

  • Ruas CF, Weiss-Schneeweiss H, Stuessy TF, Samuel MR, Pedrosa-Harand A, Tremetsberger K, Ruas PM, Schlüter PM, Ortiz Herrera MA, König C, Matzenbacher NI (2008) Characterization, genomic organization and chromosomal distribution of Ty1-copia retrotransposons in species of Hypochaeris (Asteraceae). Gene 412:39–49. doi:10.1016/j.gene.2008.01.009

    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 

  • 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, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45. doi:10.1038/1695

    Article  PubMed  CAS  Google Scholar 

  • Sant VJ, Sainani MN, Sami-Subbu R, Ranjekar PK, Gupta VS (2000) Ty1-copia retrotransposon-like elements in chickpea genome: their identification, distribution and use for diversity analysis. Gene 257:157–166. doi:10.1016/S0378-1119(00)00405-4

    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. doi:10.1073/pnas.86.13.5015

    Article  PubMed  CAS  Google Scholar 

  • Staginnus C (2001) Ph.D thesis. Department of Plant Molecular Biology, University of Frankfurt, Frankfurt

  • Staginnus C, Winter P, Desel C, Schmidt T, Kahl G (1999) Molecular structure and chromosomal localization of major repetitive DNA families in the chickpea (Cicer arietinum L.) genome. Plant Mol Biol 39:1037–1050. doi:10.1023/A:1006125430386

    Article  PubMed  CAS  Google Scholar 

  • Sugimoto K, Takeda S, Hirochika H (2000) MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. Plant Cell 12:2511–2527

    Article  PubMed  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. doi:10.1023/A:1005911413528

    Article  PubMed  CAS  Google Scholar 

  • Tapia G, Verdugo I, Yanez M, Ahumada I, Theoduloz C, Cordero C, Poblete F, Gonzalez 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. doi:10.1104/pp.105.059766

    Article  PubMed  CAS  Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815. doi:10.1038/35048692

    Article  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. doi:10.1093/nar/22.22.4673

    Article  PubMed  CAS  Google Scholar 

  • Vicient CM, Kalendar R, Anamthawat-Jonsson K, Schulman AH (1999) Structure, functionality, and evolution of the BARE-1 retrotransposon of barley. Genetica 107:53–63. doi:10.1023/A:1003929913398

    Article  PubMed  CAS  Google Scholar 

  • Warmington JR, Waring RB, Newlon CS, Indge KJ, Oliver SG (1985) Nucleotide sequence characterization of Ty 1-17, a class II transposon from yeast. Nucleic Acids Res 13:6679–6693. doi:10.1093/nar/13.18.6679

    Article  PubMed  CAS  Google Scholar 

  • Wessler SR, Bureau TE, White SE (1995) LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev 5:814–821. doi:10.1016/0959-437X(95)80016-X

    Article  PubMed  CAS  Google Scholar 

  • Wright DA, Voytas DF (1998) Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149:703–715

    PubMed  CAS  Google Scholar 

  • Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319:1527–1530. doi:10.1126/science.1153040

    Article  PubMed  CAS  Google Scholar 

  • Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3360

    PubMed  CAS  Google Scholar 

  • Ya HY, Gu YH, Jiao Z, Wang WD, Qin GY, Huo YP (2007) Low-energy ion beam promotes the transcription and transposition of the Copia-retrotransposons in wheat (Triticum aestivum L.). J plant physiol mol biol 33:507–516

    CAS  Google Scholar 

  • Zhu H, Choi H, Cook RC, Shoemaker RC (2005) Bridging model and crop legumes through comparative genomics. Plant Physiol 137:1189–1196. doi:10.1104/pp.104.058891

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to extend their sincere thanks to Dr. KR Koundal, National Research Centre on Plant Biotechnology, IARI, New Delhi, for providing chickpea genomic library. Dr. MK Rajput thanks to Council of Scientific and Industrial Research, govt. of India for fellowship.

Author information

Authors and Affiliations

  1. Molecular Genetics Laboratory, School of Life Sciences, Jawaharlal Nehru University, New Delhi, 110067, India

    Manoj K. Rajput & Kailash C. Upadhyaya

Authors
  1. Manoj K. Rajput
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kailash C. Upadhyaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manoj K. Rajput.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rajput, M.K., Upadhyaya, K.C. CARE1, a TY3-gypsy like LTR-retrotransposon in the food legume chickpea (Cicer arietinum L.). Genetica 136, 429–437 (2009). https://doi.org/10.1007/s10709-008-9343-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-008-9343-x

Keywords

Search

Navigation