Skip to main content
Log in

Identification of transposons, retroelements, and a gene family predominantly expressed in floral tissues in chromosome 3DS of the hexaploid wheat progenitor Aegilops tauschii

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

A multigene family expressed during early floral development was identified on the short arm of wheat chromosome 3D in the region of the Ph2 locus, a locus controlling homoeologous chromosome pairing in allohexaploid wheat. Physical, genetic and molecular characterisation of the Wheat Meiosis 1 (WM1) gene family identified seven members that localised within a region of 173-kb. WM1 gene family members were sequenced and they encode mainly type Ia plasma membrane-anchored leucine rich repeat-like receptor proteins. In situ expression profiling suggests the gene family is predominantly expressed in floral tissue. In addition to the WM1 gene family, a number of other genes, gene fragments and pseudogenes were identified. It has been predicted that there is approximately one gene every 19-kb and that this region of the wheat genome contains 23 repetitive elements including BARE-1 and Wis2-1 like sequences. Nearly 50% of the repetitive elements identified were similar to known transposons from the CACTA superfamily. Ty1-copia, Ty3-gypsy and Athila LTR retroelements were also prevalent within the region. The WM1 gene cluster is present on 3DS and on barley 3HS but missing from the A and B genomes of hexaploid wheat. This suggests either recent generation of the cluster or specific deletion of the cluster during wheat polyploidisation. The evolutionary significance of the cluster, its possible roles in disease response or floral and early meiotic development and its location at or near the Ph2 locus are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

LRR:

Leucine-rich repeat

RLKs:

Receptor-like kinases

RLPs:

Receptor-like proteins

ORF:

Open reading frame

Ph :

Pairing homoeologous

TtBAC :

Aegilops tauschii bacterial artificial chromosome

WM :

Wheat meiosis

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, 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 

  • Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, Bucher P, Cerutti L, Corpet F, Croning MD, Durbin R, Falquet L, Fleischmann W, Gouzy J, Hermjakob H, Hulo N, Jonassen I, Kahn D, Kanapin A, Karavidopoulou Y, Lopez R, Marx B, Mulder NJ, Oinn TM, Pagni M, Servant F (2001) The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 29:37–40

    Article  Google Scholar 

  • Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884

    Article  PubMed  CAS  Google Scholar 

  • Barakat A, Carels N, Bernardi G (1997) The distribution of genes in the genomes of Gramineae. Proc Natl Acad Sci U S A 94:6857–6861

    Article  PubMed  CAS  Google Scholar 

  • Barr AR, Chalmers KJ, Karakousis A, Kretschmer JM, Manning S, Lance RCM, Lewis J, Jefferies SP, Langridge P (1998) RFLP mapping of a new cereal cyst nematode resistance locus in barley. Plant Breed 117:185–187

    Article  Google Scholar 

  • Becraft PW (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18:163–192

    Article  PubMed  CAS  Google Scholar 

  • Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447

    Article  PubMed  CAS  Google Scholar 

  • Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germ line cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727

    Article  PubMed  CAS  Google Scholar 

  • Comeron JM (1999) K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15:763–764

    Article  PubMed  CAS  Google Scholar 

  • Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451–459

    Article  PubMed  CAS  Google Scholar 

  • Dong C, Whitford R, Langridge P (2002) A DNA mismatch repair gene links to the Ph2 locus in wheat. Genome 45:116–124

    Article  PubMed  CAS  Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    Article  PubMed  CAS  Google Scholar 

  • Fritz-Laylin LK, Krishnamurthy N, Tor M, Sjolander KV, Jones JD (2005) Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol 138:611–623

    Article  PubMed  CAS  Google Scholar 

  • Gay NJ, Packman LC, Weldon MA, Barna JCJ (1991) A leucine-rich repeat peptide derived from the Drosophila toll receptor forms extended filaments with b-sheet structure. FEBS Lett 291:87–91

    Article  PubMed  CAS  Google Scholar 

  • Gonzáles-Gaitán M (2003) Signal dispersal and transduction through the endocytic pathway. Nature Rev Mol Cell Biol 4:213–224

    Article  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) CONSED—a graphical tool for sequence finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • Hofmann K, Stoffel W (1993) TMbase—A database of membrane spanning proteins segments. Biol Chem Hoppe Seyler 374:166

    Google Scholar 

  • Hofmann K, Bucher P, Falquet L, Bairoch A (1999) The PROSITE database, its status in 1999. Nucleic Acids Res 27:215–219

    Article  PubMed  CAS  Google Scholar 

  • Huang Y, Zhang L (2004) Rapid and sensitive dot-matrix methods for genome analysis. Bioinformatics 20:460–466

    Article  PubMed  CAS  Google Scholar 

  • Hulbert SH (1997) Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu Rev Phytopathol 35:293–310

    Article  PubMed  CAS  Google Scholar 

  • Hyatt D, Snoddy J, Schmoyer D, Chen G, Fischer K, Parang M, Vokler I, Petrov S, Locascio P, Olman V, Land M, Shah M, Uberbacher E (2000a) GRAIL-EXP and the genome analysis toolkit. In: The 13th annual Cold Spring Harbor meeting on genome sequencing and biology, Cold Spring Harbor, New York, 10–14 May 2000

  • Hyatt D, Snoddy J, Schmoyer D, Chen G, Fischer K, Parang M, Vokler I, Petrov S, Locascio P, Olman V, Land M, Shah M, Uberbacher E (2000b) Improved analysis and annotation tools for whole-genome computational annotation and analysis: GRAIL-EXP genome analysis toolkit and related analysis tools. In: The 13th annual Cold Spring Harbor meeting on genome sequencing and biology, Cold Spring Harbor, New York, 10–14 May 2000

  • Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–1933

    Article  Google Scholar 

  • Ji LH (1992) A study of meiosis in allohexaploid wheat: the molecular aspects. Thesis, University of Adelaide

  • Ji LH, Langridge P (1994) An early meiosis cDNA clone from wheat. Mol Gen Genet 243:17–23

    Article  PubMed  CAS  Google Scholar 

  • Jones DA, Jones JDG (1997) The roles of leucine-rich repeat proteins in plant defences. Advances in Botanical Research incorporating Advances in Plant Pathology 24:89–167

    Google Scholar 

  • Jones DA, Thomas CM, Hammond-Kosack KE, Balintkurti PJ, Jones JDG (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793

    Article  PubMed  CAS  Google Scholar 

  • Juttner J, Olde D, Langridge P, Baumann U (2000) Cloning and expression of a distinct subclass of plant thioredoxins. Eur J Biochem 267:7109–7117

    Article  PubMed  CAS  Google Scholar 

  • Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci U S A 98:6511–6515

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171

    Article  PubMed  CAS  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  PubMed  CAS  Google Scholar 

  • Kruijt M, De-Kock MJD, de-Wit PJGM (2005) Receptor-like proteins involved in plant disease resistance. Mol Plant Pathol 6:85–97

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lamacchia C, Shewry PR, Di Fonzo N, Forsyth JL, Harris N, Lazzeri PA, Napier JA, Halford NG, Barcelo P (2001) Endosperm-specific activity of a storage protein gene promoter in transgenic wheat seed. J Exp Bot 52:243–250

    Article  PubMed  CAS  Google Scholar 

  • Lescot M, Rombauts S, Zhang J, Aubourg S, Mathe C, Janssson S, Rouze P, Boerjan W (2004) Annotation of a 95-kb Populus deltoides genomic sequence reveals a disease resistance gene cluster and novel class I and class II transposable elements. Theor Appl Genet 109:10–22

    Article  PubMed  CAS  Google Scholar 

  • Letourneur F, Klausner RD (1992) A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69:1143–1157

    Article  PubMed  CAS  Google Scholar 

  • Li HY, Gray JE (1997) Pollination-enhanced expression of a receptor-like protein kinase related gene in tobacco styles. Plant Mol Biol 33:653–665

    Article  PubMed  CAS  Google Scholar 

  • Maliga P, Klessig DF, Cashmore AR, Gruissem W, Varner JE (1995) Methods in plant molecular biology: a laboratory course manual. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Manly KF, Olson JM (1999) Overview of QTL mapping software and introduction to map manager QT. Mamm Genome 10:327–334

    Article  PubMed  CAS  Google Scholar 

  • Marks MS, Woodruff L, Ohno H, Bonifacino JS (1996) Protein targeting by tyrosine- and di-leucine-based signals: evidence for distinct saturable components. J Cell Biol 135:341–354

    Article  PubMed  CAS  Google Scholar 

  • Matsubayashi Y (2003) Ligand-receptor pairs in plant peptide signaling. J Cell Sci 116:3863–3870

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  PubMed  CAS  Google Scholar 

  • Moullet O, Zhang HB, Lagudah ES (1999) Construction and characterisation of a large DNA insert library from the D genome of wheat. Theor Appl Genet 99:305–313

    Article  Google Scholar 

  • Muschietti J, Eyal Y, McCormick S (1998) Pollen tube localization implies a role in pollen-pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell 10:319–330

    Article  PubMed  CAS  Google Scholar 

  • Nadeau JA, Sack FD (2002) Control of stomatal distribution on the Arabidopsis leaf surface. Science 296:1697–1700

    Article  PubMed  CAS  Google Scholar 

  • Nakai K, Kanehisa M (1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14:897–911

    Article  PubMed  CAS  Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  PubMed  CAS  Google Scholar 

  • Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1739

    Article  PubMed  CAS  Google Scholar 

  • Parniske M, Jones JDG (1999) Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proc Natl Acad Sci U S A 96:5850–5855

    Article  PubMed  CAS  Google Scholar 

  • Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BBH, Jones JDG (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821–832

    Article  PubMed  CAS  Google Scholar 

  • Parniske M, Wulff BBH, Bonnema G, Thomas CM, Jones DA, Jones JDG (1999) Homologues of the Cf-9 disease resistance gene (Hcr9s) are present at multiple loci on the short arm of tomato chromosome 1. Mol Plant Microbe Interact 12:93–102

    PubMed  CAS  Google Scholar 

  • QIAGEN (1998) The QIAGEN guide to template purification and DNA sequencing. QIAGEN, Australia

    Google Scholar 

  • Rechsteiner M, Rogers SW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21:267–271

    Article  PubMed  CAS  Google Scholar 

  • Rogers SW, Wells R, Rechsteiner M (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234:364–368

    Article  PubMed  CAS  Google Scholar 

  • Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615

    Article  PubMed  CAS  Google Scholar 

  • Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, Chory J, de Vries SC (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216–3229

    Article  PubMed  CAS  Google Scholar 

  • Sambrook F, Fritsch EF, Maniatis F (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Sears ER (1977) An induced mutant with homoeologous pairing in common wheat. Can J Genet Cytol 19:585–593

    Google Scholar 

  • Sears ER (1982) A wheat mutant conditioning an intermediate level of homoeologous chromosome pairing. Can J Genet Cytol 24:715–719

    Google Scholar 

  • Shui SH, Bleeker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A 98:10763–10768

    Article  Google Scholar 

  • Suoniemi A, Narvanto A, Schulman AH (1996) The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol Biol 31:295–306

    Article  PubMed  CAS  Google Scholar 

  • Sutton T, Whitford R, Baumann U, Dong C, Able JA, Langridge P (2003) The Ph2 pairing homoeologous locus of wheat (Triticum aestivum): identification of candidate meiotic genes using a comparative genetics approach. Plant J 36:443–456

    Article  PubMed  CAS  Google Scholar 

  • Suzuki N, Choe HR, Nishida Y, Yamawaki-Kataoka Y, Ohnishi S, Tamaoki T, Kataoka T (1990) Leucine-rich repeats and carboxyl terminus are required for interaction of yeast adenylate cyclase with RAS proteins. Proc Natl Acad Sci U S A 87:8711–8715

    Article  PubMed  CAS  Google Scholar 

  • Taguchi-Shiobara F, Yuan Z, Hake S, Jackson D (2001) The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev 15:2755–2766

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Mu JH, Gasch A, Chua NH (1998) Identification by PCR of receptor-like protein kinases from Arabidopsis flowers. Plant Mol Biol 37:587–596

    Article  PubMed  CAS  Google Scholar 

  • Talbert PB, Bryson TD, Henikoff S (2004) Adaptive evolution of centromere proteins in plants and animals. J Biol 3:18

    Article  PubMed  Google Scholar 

  • Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti P, Hatzixanthis K, Jones JDG (1997) Characterisation of the Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209–2224

    Article  PubMed  CAS  Google Scholar 

  • Thomas CM, Dixon MS, Parniske M, Golstein C, Jones JD (1998) Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum. Philos Trans R Soc Lond B Biol Sci 353:1413–1424

    Article  PubMed  CAS  Google Scholar 

  • Tor M, Brown D, Cooper A, Woods-Tor A, Sjolander K, Jones JD, Holub EB (2004) Arabidopsis downy mildew resistance gene RPP27 encodes a receptor-like protein similar to CLAVATA2 and tomato Cf-9. Plant Physiol 135:1100–1112

    Article  PubMed  Google Scholar 

  • Vicient CM, Jaaskelainen MJ, Kalendar R, Schulman AH (2001) Active retrotransposons are a common feature of grass genomes. Plant Physiol 125:1283–1292

    Article  PubMed  CAS  Google Scholar 

  • Vinatzer BA, Patocchi A, Gianfranceschi L, Tartarini S, Zhang HB, Gessler C, Sansavini S (2001) Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes co-segregating with Vf apple scab resistance. Mol Plant Microbe Interact 14:508–515

    PubMed  CAS  Google Scholar 

  • von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683–4690

    Google Scholar 

  • Wicker T, Zimmermann W, Perovic D, Paterson AH, Ganal M, Graner A, Stein N (2005) A detailed look at 7 million years of genome evolution in a 439 kb contiguous sequence at the barley Hv-elF4E locus: recombination, rearrangements and repeats. Plant J 41:184–194

    Article  PubMed  CAS  Google Scholar 

  • Yang M, Sack FD (1995) The too many mouths and four lips mutations affect stomatal production in Arabidopsis. Plant Cell 7:2227–2239

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Thomas Wicker of the Institute of Plant Biology, University of Zürich for sequence analysis support. RW was funded through GRDC with additional support from Agriculture Western Australia. The authors gratefully acknowledge the Molecular Plant Breeding Cooperative Research Centre and the Australian Research Council (Special Research Centre for Basic and Applied Plant Molecular Biology), for funding this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jason A. Able.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Whitford, R., Baumann, U., Sutton, T. et al. Identification of transposons, retroelements, and a gene family predominantly expressed in floral tissues in chromosome 3DS of the hexaploid wheat progenitor Aegilops tauschii . Funct Integr Genomics 7, 37–52 (2007). https://doi.org/10.1007/s10142-006-0026-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-006-0026-3

Keywords

Navigation