• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Mar 2004; 166(3): 1437–1450.
PMCID: PMC1470764

Large retrotransposon derivatives: abundant, conserved but nonautonomous retroelements of barley and related genomes.

Abstract

Retroviruses and LTR retrotransposons comprise two long-terminal repeats (LTRs) bounding a central domain that encodes the products needed for reverse transcription, packaging, and integration into the genome. We describe a group of retrotransposons in 13 species and four genera of the grass tribe Triticeae, including barley, with long, approximately 4.4-kb LTRs formerly called Sukkula elements. The approximately 3.5-kb central domains include reverse transcriptase priming sites and are conserved in sequence but contain no open reading frames encoding typical retrotransposon proteins. However, they specify well-conserved RNA secondary structures. These features describe a novel group of elements, called LARDs or large retrotransposon derivatives (LARDs). These appear to be members of the gypsy class of LTR retrotransposons. Although apparently nonautonomous, LARDs appear to be transcribed and can be recombinationally mapped due to the polymorphism of their insertion sites. They are dispersed throughout the genome in an estimated 1.3 x 10(3) full-length copies and 1.16 x 10(4) solo LTRs, indicating frequent recombinational loss of internal domains as demonstrated also for the BARE-1 barley retrotransposon.

Full Text

The Full Text of this article is available as a PDF (863K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bonhoeffer S, McCaskill JS, Stadler PF, Schuster P. RNA multi-structure landscapes. A study based on temperature dependent partition functions. Eur Biophys J. 1993;22(1):13–24. [PubMed]
  • Boyko Elena, Kalendar Ruslan, Korzun Victor, Fellers John, Korol Abraham, Schulman Alan H, Gill Bikram S. A high-density cytogenetic map of the Aegilops tauschii genome incorporating retrotransposons and defense-related genes: insights into cereal chromosome structure and function. Plant Mol Biol. 2002 Mar-Apr;48(5-6):767–790. [PubMed]
  • Casacuberta JM, Vernhettes S, Grandbastien MA. Sequence variability within the tobacco retrotransposon Tnt1 population. EMBO J. 1995 Jun 1;14(11):2670–2678. [PMC free article] [PubMed]
  • Driscoll MD, Golinelli MP, Hughes SH. In vitro analysis of human immunodeficiency virus type 1 minus-strand strong-stop DNA synthesis and genomic RNA processing. J Virol. 2001 Jan;75(2):672–686. [PMC free article] [PubMed]
  • Flavell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R, Kumar A. Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res. 1992 Jul 25;20(14):3639–3644. [PMC free article] [PubMed]
  • Manninen O, Kalendar R, Robinson J, Schulman AH. Application of BARE-1 retrotransposon markers to the mapping of a major resistance gene for net blotch in barley. Mol Gen Genet. 2000 Oct;264(3):325–334. [PubMed]
  • Frankel AD, Young JA. HIV-1: fifteen proteins and an RNA. Annu Rev Biochem. 1998;67:1–25. [PubMed]
  • Marquet R, Isel C, Ehresmann C, Ehresmann B. tRNAs as primer of reverse transcriptases. Biochimie. 1995;77(1-2):113–124. [PubMed]
  • Friant S, Heyman T, Wilhelm FX, Wilhelm M. Role of RNA primers in initiation of minus-strand and plus-strand DNA synthesis of the yeast retrotransposon Ty1. Biochimie. 1996;78(7):674–680. [PubMed]
  • McAllister BF, Werren JH. Phylogenetic analysis of a retrotransposon with implications for strong evolutionary constraints on reverse transcriptase. Mol Biol Evol. 1997 Jan;14(1):69–80. [PubMed]
  • Meyers BC, Tingey SV, Morgante M. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 2001 Oct;11(10):1660–1676. [PMC free article] [PubMed]
  • Hartl DL, Lozovskaya ER, Lawrence JG. Nonautonomous transposable elements in prokaryotes and eukaryotes. Genetica. 1992;86(1-3):47–53. [PubMed]
  • Monfort A, Vicient CM, Raz R, Puigdomènech P, Martínez-Izquierdo JA. Molecular analysis of a putative transposable retroelement from the Zea genus with internal clusters of tandem repeats. DNA Res. 1995 Dec 31;2(6):255–261. [PubMed]
  • Heidmann T, Heidmann O, Nicolas JF. An indicator gene to demonstrate intracellular transposition of defective retroviruses. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2219–2223. [PMC free article] [PubMed]
  • Peleg Ofer, Brunak Søren, Trifonov Edward N, Nevo Eviatar, Bolshoy Alexander. RNA secondary structure and squence conservation in C1 region of human immunodeficiency virus type 1 env gene. AIDS Res Hum Retroviruses. 2002 Aug 10;18(12):867–878. [PubMed]
  • Higgins DG, Thompson JD, Gibson TJ. Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 1996;266:383–402. [PubMed]
  • Petersen G, Seberg O. Phylogenetic analysis of the Triticeae (Poaceae) based on rpoA sequence data. Mol Phylogenet Evol. 1997 Apr;7(2):217–230. [PubMed]
  • Hofacker Ivo L, Fekete Martin, Stadler Peter F. Secondary structure prediction for aligned RNA sequences. J Mol Biol. 2002 Jun 21;319(5):1059–1066. [PubMed]
  • Hsiao C, Chatterton NJ, Asay KH, Jensen KB. Phylogenetic relationships of the monogenomic species of the wheat tribe, Triticeae (Poaceae), inferred from nuclear rDNA (internal transcribed spacer) sequences. Genome. 1995 Apr;38(2):211–223. [PubMed]
  • SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, et al. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996 Nov 1;274(5288):765–768. [PubMed]
  • Hudakova S, Michalek W, Presting GG, ten Hoopen R, dos Santos K, Jasencakova Z, Schubert I. Sequence organization of barley centromeres. Nucleic Acids Res. 2001 Dec 15;29(24):5029–5035. [PMC free article] [PubMed]
  • Schneider TD, Stephens RM. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 1990 Oct 25;18(20):6097–6100. [PMC free article] [PubMed]
  • Schneider TD, Stormo GD, Gold L, Ehrenfeucht A. Information content of binding sites on nucleotide sequences. J Mol Biol. 1986 Apr 5;188(3):415–431. [PubMed]
  • Jaeger JA, Turner DH, Zuker M. Predicting optimal and suboptimal secondary structure for RNA. Methods Enzymol. 1990;183:281–306. [PubMed]
  • Schultz SJ, Zhang M, Kelleher CD, Champoux JJ. Analysis of plus-strand primer selection, removal, and reutilization by retroviral reverse transcriptases. J Biol Chem. 2000 Oct 13;275(41):32299–32309. [PubMed]
  • Jiang Ning, Bao Zhirong, Temnykh Svetlana, Cheng Zhukuan, Jiang Jiming, Wing Rod A, McCouch Susan R, Wessler Susan R. Dasheng: a recently amplified nonautonomous long terminal repeat element that is a major component of pericentromeric regions in rice. Genetics. 2002 Jul;161(3):1293–1305. [PMC free article] [PubMed]
  • Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P. A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res. 2000 Jul;10(7):908–915. [PMC free article] [PubMed]
  • Jiang Ning, Jordan I King, Wessler Susan R. Dasheng and RIRE2. A nonautonomous long terminal repeat element and its putative autonomous partner in the rice genome. Plant Physiol. 2002 Dec;130(4):1697–1705. [PMC free article] [PubMed]
  • Siebert PD, Chenchik A, Kellogg DE, Lukyanov KA, Lukyanov SA. An improved PCR method for walking in uncloned genomic DNA. Nucleic Acids Res. 1995 Mar 25;23(6):1087–1088. [PMC free article] [PubMed]
  • Suoniemi A, Anamthawat-Jónsson K, Arna T, Schulman AH. Retrotransposon BARE-1 is a major, dispersed component of the barley (Hordeum vulgare L.) genome. Plant Mol Biol. 1996 Mar;30(6):1321–1329. [PubMed]
  • Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6603–6607. [PMC free article] [PubMed]
  • Suoniemi A, Schmidt D, Schulman AH. BARE-1 insertion site preferences and evolutionary conservation of RNA and cDNA processing sites. Genetica. 1997;100(1-3):219–230. [PubMed]
  • Suoniemi A, Tanskanen J, Schulman AH. Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J. 1998 Mar;13(5):699–705. [PubMed]
  • Kerwood DJ, Cavaluzzi MJ, Borer PN. Structure of SL4 RNA from the HIV-1 packaging signal. Biochemistry. 2001 Dec 4;40(48):14518–14529. [PubMed]
  • Suoniemi A, Tanskanen J, Pentikäinen O, Johnson MS, Schulman AH. The core domain of retrotransposon integrase in Hordeum: predicted structure and evolution. Mol Biol Evol. 1998 Sep;15(9):1135–1144. [PubMed]
  • Thompson JD, Higgins DG, Gibson TJ. 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 Nov 11;22(22):4673–4680. [PMC free article] [PubMed]
  • Kumar A, Bennetzen JL. Plant retrotransposons. Annu Rev Genet. 1999;33:479–532. [PubMed]
  • Kumekawa N, Ohtsubo H, Horiuchi T, Ohtsubo E. Identification and characterization of novel retrotransposons of the gypsy type in rice. Mol Gen Genet. 1999 Jan;260(6):593–602. [PubMed]
  • Vicient CM, Suoniemi A, Anamthawat-Jónsson K, Tanskanen J, Beharav A, Nevo E, Schulman AH. Retrotransposon BARE-1 and Its Role in Genome Evolution in the Genus Hordeum. Plant Cell. 1999 Sep;11(9):1769–1784. [PMC free article] [PubMed]
  • Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004 Dec 9;432(7018):695–716. [PubMed]
  • Vicient CM, Jäskeläinen MJ, Kalendar R, Schulman AH. Active retrotransposons are a common feature of grass genomes. Plant Physiol. 2001 Mar;125(3):1283–1292. [PMC free article] [PubMed]
  • Yang J, Bogerd H, Le SY, Cullen BR. The human endogenous retrovirus K Rev response element coincides with a predicted RNA folding region. RNA. 2000 Nov;6(11):1551–1564. [PMC free article] [PubMed]
  • Zeeberg Barry. Shannon information theoretic computation of synonymous codon usage biases in coding regions of human and mouse genomes. Genome Res. 2002 Jun;12(6):944–955. [PMC free article] [PubMed]
  • Voytas DF, Cummings MP, Koniczny A, Ausubel FM, Rodermel SR. copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7124–7128. [PMC free article] [PubMed]
  • Zuker M. On finding all suboptimal foldings of an RNA molecule. Science. 1989 Apr 7;244(4900):48–52. [PubMed]
  • Wicker T, Stein N, Albar L, Feuillet C, Schlagenhauf E, Keller B. Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J. 2001 May;26(3):307–316. [PubMed]
  • Zuker M. Prediction of RNA secondary structure by energy minimization. Methods Mol Biol. 1994;25:267–294. [PubMed]
  • Zuker M, Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981 Jan 10;9(1):133–148. [PMC free article] [PubMed]
  • Witte CP, Le QH, Bureau T, Kumar A. Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13778–13783. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...