Skip to main content

Updating of transposable element annotations from large wheat genomic sequences reveals diverse activities and gene associations

Abstract

Triticeae species (including wheat, barley and rye) have huge and complex genomes due to polyploidization and a high content of transposable elements (TEs). TEs are known to play a major role in the structure and evolutionary dynamics of Triticeae genomes. During the last 5 years, substantial stretches of contiguous genomic sequence from various species of Triticeae have been generated, making it necessary to update and standardize TE annotations and nomenclature. In this study we propose standard procedures for these tasks, based on structure, nucleic acid and protein sequence homologies. We report statistical analyses of TE composition and distribution in large blocks of genomic sequences from wheat and barley. Altogether, 3.8 Mb of wheat sequence available in the databases was analyzed or re-analyzed, and compared with 1.3 Mb of re-annotated genomic sequences from barley. The wheat sequences were relatively gene-rich (one gene per 23.9 kb), although wheat gene-derived sequences represented only 7.8% (159 elements) of the total, while the remainder mainly comprised coding sequences found in TEs (54.7%, 751 elements). Class I elements [mainly long terminal repeat (LTR) retrotransposons] accounted for the major proportion of TEs, in terms of sequence length as well as element number (83.6% and 498, respectively). In addition, we show that the gene-rich sequences of wheat genome A seem to have a higher TE content than those of genomes B and D, or of barley gene-rich sequences. Moreover, among the various TE groups, MITEs were most often associated with genes: 43.1% of MITEs fell into this category. Finally, the TRIM and copia elements were shown to be the most active TEs in the wheat genome. The implications of these results for the evolution of diploid and polyploid wheat species are discussed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Altschul SF, Madden TL, Schäffer 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

    Article  PubMed  CAS  Google Scholar 

  • Anderson OD, Rausch C, Moullet O, Lagudah ES (2003) The wheat D-genome HMW-glutenin locus: BAC sequencing, gene distribution, and retrotransposon clusters. Funct Integr Genomics 3:56–68

    PubMed  CAS  Google Scholar 

  • Bendich AJ, McCarthy BJ (1970) DNA comparisons among barley, oats, rye, and wheat. Genetics 65:545–565

    PubMed  CAS  Google Scholar 

  • Bennett MD, Leitch IJ (1995) Nuclear DNA amounts in angiosperms. Ann Bot 76:113–176

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132

    Article  PubMed  CAS  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  PubMed  CAS  Google Scholar 

  • Blanco E, Parra G, Guigo R (2002) Using GeneID to identify genes. Current protocols in bioinformatics. Wiley, New York

    Book  Google Scholar 

  • Brooks SA, Huang L, Gill BS, Fellers JP (2002) Analysis of 106 kb of contiguous DNA sequence from the D genome of wheat reveals high gene density and a complex arrangement of genes related to disease resistance. Genome 45:963–972

    Article  PubMed  CAS  Google Scholar 

  • Bureau TE, Wessler SR (1994a) Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc Natl Acad Sci USA 91:1411–1415

    PubMed  Article  CAS  Google Scholar 

  • Bureau TE, Wessler SR (1994b) Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell 6:907–916

    Article  PubMed  CAS  Google Scholar 

  • Chantret N et al (2005) Molecular basis of evolutionary events that shaped the Hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:1033–1045

    Article  PubMed  CAS  Google Scholar 

  • Chantret N, Cenci A, Sabot F, Anderson O, Dubcovsky J (2004) Sequencing of the Triticum monococcum Hardness locus reveals good microcolinearity with rice. Mol Genet Genomics 271:377–386

    Article  PubMed  CAS  Google Scholar 

  • Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079

    Article  PubMed  CAS  Google Scholar 

  • Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol 125:1342–1353

    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

    Article  PubMed  CAS  Google Scholar 

  • Feuillet C, Keller B (1999) High gene density is conserved at syntenic loci of small and large grass genomes. Proc Natl Acad Sci USA 96:8265–8270

    Article  PubMed  CAS  Google Scholar 

  • Feuillet C, Penger A, Gellner K, Mast A, Keller B (2001) Molecular evolution of receptor-like kinase genes in hexaploid wheat. Independent evolution of orthologs after polyploidization and mechanisms of local rearrangements at paralogous loci. Plant Physiol 125:1304–1313

    Article  PubMed  CAS  Google Scholar 

  • Flavell RB, Rimpau J, Smith DB (1977) Repeated sequence DNA relationship in four cereals genomes. Chromosoma 63:205–222

    Article  CAS  Google Scholar 

  • Gu YQ, Coleman-Derr DA, Kong X, Anderson OD (2004) Rapid genome evolution revealed by comparative analysis of orthologous regions from four Triticeae genomes. Plant Physiol 135:459–470

    Article  PubMed  CAS  Google Scholar 

  • Hu J, Reddy VS, Wessler SR (2000) The rice R gene family: two distinct subfamilies containing several miniature inverted-repeat transposable elements. Plant Mol Biol 42:667–678

    Article  PubMed  CAS  Google Scholar 

  • Huang S, Sirikhachornkit A, Faris JD, Su X, Gill BS, Haselkorn R, Gornicki P (2002) Phylogenetic analysis of the acetyl-CoA carboxylase and 3-phosphoglycerate kinase loci in wheat and other grasses. Plant Mol Biol 48:805–820

    Article  PubMed  CAS  Google Scholar 

  • Huang L, Brooks SA, Wanlong L, Fellers JP, Trick HN, Gill BS (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics 164:655–664

    PubMed  CAS  Google Scholar 

  • Iwamoto M, Higo K (2003) Tourist C transposable elements are closely associated with genes expressed in flowers in rice (Oryza sativa). Mol Genet Genomics 268:771–778

    PubMed  CAS  Google Scholar 

  • Jiang N, Wessler SR (2001) Insertion preference of maize and rice miniature inverted repeat transposable elements as revealed by the analysis of nested element. Plant Cell 13:2553–2564

    Article  PubMed  CAS  Google Scholar 

  • Juretic N, Bureau TE, Bruskiewich RM (2004) Transposable elements annotation of the rice genome. Bioinformatics 20:155–160

    Article  PubMed  CAS  Google Scholar 

  • Jurka J (1997) Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci USA 94:1872–1877

    Article  PubMed  CAS  Google Scholar 

  • Jurka J (2000) RepBase update: a database and an electronic journal of repetitive elements. Trends Genet 16:418–420

    Article  PubMed  CAS  Google Scholar 

  • Kalendar R, Vicient CM, Peleg O, Anamthawat-Jonsson K, Bolshoy A, Schulman AH (2004) LArge retrotransposon derivatives: abundant, conserved but non-autonomous retroelements of barley and related genomes. Genetics 166:1437–1450

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci USA 98:8714–8719

    Article  PubMed  CAS  Google Scholar 

  • Keller B, Feuillet C (2000) Colinearity and gene density in grass genomes. Trends Plant Sci 5:246–251

    Article  PubMed  CAS  Google Scholar 

  • Kong X-Y, Gu YQ, You FM, Dubcovsky J, Anderson OD (2004) Dynamics of the evolution of orthologous and paralogous portions of a complex locus region in two genomes of allopolyploid wheat. Plant Mol Biol 54:55–69

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lal SK, Giroux MJ, Brendel V, Vallejos CE, Hannah LC (2003) The maize genome contains a Helitron insertion. Plant Cell 15:381–391

    Article  PubMed  CAS  Google Scholar 

  • Levy AA, Feldman M (2002) The impact of polyploidy on grass genome evolution. Plant Physiol 130:1587–1593

    Article  PubMed  CAS  Google Scholar 

  • Li W, Zhang P, Fellers JP, Friebe B, Gill BS (2004) Sequence composition, organization and evolution of the core Triticeae genome. Plant J 40:500–511

    Article  PubMed  CAS  Google Scholar 

  • Lijavetzky D, Muzzi G, Wicker T, Keller B, Wing R, Dubcovsky J (1999) Construction and characterization of a bacterial artificial chromosome (BAC) library for the A genome of wheat. Genome 42:1176–1182

    Article  PubMed  CAS  Google Scholar 

  • Lukashin AV, Borodovsky M (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26:1107–1115

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869

    Article  PubMed  CAS  Google Scholar 

  • Mao L, Wood TC, Yu Y, Budiman MA, Tomkins J, Woo S-S, Sasinwski M, Presting G, Frisch D, Goff S, Dean RA, Wing RA (2000) Rice transposable elements: a survey of 73,000 sequence-tagged-connectors. Genome Res 10:982–990

    Article  PubMed  CAS  Google Scholar 

  • McCarthy EM, McDonald JF (2003) LTR_STRUC: a novel search and identification program for LTR retrotransposons. Bioinformatics 19:362–367

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676

    Article  PubMed  CAS  Google Scholar 

  • Rahman S, Abrahams S, Abbot D, Mukai Y, Samuel M, Morell M, Appels R (1997) A complex arrangement of genes at a starch branching enzyme I locus in the D-genome donor of wheat. Genome 40:465–474

    PubMed  CAS  Google Scholar 

  • Rutherford K, Parkhill J, Crook JHT, Rice P, Rajandream M-A, Barrell B (2000) ARTEMIS: sequence visualisation and annotation. Bioinformatics 16:944–945

    Article  PubMed  CAS  Google Scholar 

  • Sabot F, Simon D, Bernard M (2004) Plant transposable elements, with an emphasis on grass species. Euphytica 139:227–247

    Article  CAS  Google Scholar 

  • Salamini F, Ozkan H, Brandolini A, Schafer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the near east. Nat Rev Genet 3:429–441

    PubMed  CAS  Google Scholar 

  • Sandhu D, Gill KS (2002) Gene-containing regions of wheat and the other grass genomes. Plant Physiol 128:803–8011

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin Y-K, 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 the maize genome. Science 274:765–768

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel P, Ramakrishna W, Bennetzen JL, Busso C, Dubcovsky J (2002) Transposable elements, genes and recombination in a 215-kb contig from wheat chromosome 5Am. Funct Integr Genom 2:70–80

    Article  CAS  Google Scholar 

  • Sonnhammer ELL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:1–10

    Article  PubMed  Google Scholar 

  • Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons. Mol Biol Evol 20:528–540

    Article  PubMed  CAS  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Stein N, Albar L, Feuillet C, Schlagenhauf E, Keller B (2001) Analysis of a 211-kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J 26:307–316

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Matthews DE, Keller B (2002) TREP: a database for Triticeae REPetitive elements. Trends Plant Sci 7:561–562

    Article  CAS  Google Scholar 

  • Wicker T, Yahiaoui N, Guyot R, Schlagenhauf E, Liu Z-D, Dubcovsky J, Keller B (2003a) Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat. Plant Cell 15:1186–1197

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Guyot R, Yahiaoui N, Keller B (2003b) CACTA transposons in Triticeae. A diverse family of high-copy repetitive elements. Plant Physiol 132:52–63

    Article  PubMed  CAS  Google Scholar 

  • Witte C-P, Le QH, Bureau TE, Kumar A (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 98:13778–13783

    Article  PubMed  CAS  Google Scholar 

  • Wright DA, Voytas DF (2002) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12:122–131

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Echenique V, Busso C, SanMiguel P, Ramakrishna W, Bennetzen JL, Harrington S, Dubcovsky J (2002) Cereal genes similar to Snf2 define a new subfamily that includes human and mouse genes. Mol Genet Genomics 268:488–499

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Catherine Feuillet and Beat Keller for their corrections and their “bloody cuts”, Alan Schulman for his help on the activity index and his corrections, Jorge Dubcovsky, the reviewers and the editor for their constructive observations and Bikram Gill, John Fellers, Dave Matthews and all the corresponding authors of the previous articles on large genomic sequences for their help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michel Bernard.

Additional information

Communicated by R. Hagemann

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sabot, F., Guyot, R., Wicker, T. et al. Updating of transposable element annotations from large wheat genomic sequences reveals diverse activities and gene associations. Mol Genet Genomics 274, 119–130 (2005). https://doi.org/10.1007/s00438-005-0012-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-005-0012-9

Keywords

  • Transposable elements
  • Sequence annotation
  • Triticeae
  • Genome evolution