Skip to main content
Log in

Recruitment of closely linked genes for divergent functions: the seed storage protein (Glu-3) and powdery mildew (Pm3) genes in wheat (Triticum aestivum L.)

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

Abstract

Wheat seed storage protein gene loci (Glu-3) and powdery mildew resistance gene loci (Pm3 and Pm3-like) are closely linked on the short arms of homoeologous group 1 chromosomes. To study the structural organization of the Glu-3/Pm3 loci, three bacterial artificial chromosome clones were sequenced from the A, B, and D genomes of hexaploid wheat. The A and B genome clones contained a Glu-3 adjacent to a Pm3-like gene organized in a conserved Glu-3/SFR159/Pm3-like structure. The D genome clone contained clusters of resistance gene analogs but no Pm3. Its similarity to the A and B genome was limited to the Glu-3/SFR159 region. Comparison of the B genome PM3-like deduced amino acid sequence with known PM3 functional isotypes reinforced the hypothesis of allelic evolution via block exchange by gene conversion/recombination. The advent of glutenin genes and the formation of the Glu-3/SFR159/Pm3 locus occurred after divergence of wheat from rice and Brachypodium. Comparison of the A genome homologous sequences permitted an estimate of time of divergence of ~0.3 million years ago. The B genome sequences were not colinear indicating that they could either be paralogs or represent different B genome progenitors. Analysis of the 11 complete retrotransposons indicated a time of divergence ranging from 0.29 to 5.62 million years ago, consistent with their complex nested structure.

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

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Anderson O, Dubcovsky J, Matthews D, Sabot F, Wicker T (2005) Nomenclature, classification and annotation of repetitive elements. http://wheat.pw.usda.gov/ITMI/Repeats/Nomenclatures_for_TREP.html

  • Bossolini E, Wicker T, Knobel PA, Keller B (2007) Comparison of orthologous loci from small grass genomes Brachypodium and rice: implications for wheat genomics and grass genome annotation. Plant J 49:704–717

    Article  CAS  PubMed  Google Scholar 

  • Briggle LW, Sears ER (1966) Linkage of resistance to Erysiphe graminis f. sp. tritici (Pm3) and hairy glume (Hg) on chromosome 1A of wheat. Crop Sci 6:559–562

    Article  Google Scholar 

  • Brodie R, Roper RL, Upton C (2004) J Dotter: a Java interface to multiple dotplots generated by dotter. Bioinformatics 20:279–281

    Article  CAS  PubMed  Google Scholar 

  • Cassidy BG, Dvorak J, Anderson OD (1998) The wheat low molecular-weight glutenin genes: characterization of six new genes and progress in understanding gene family structure. Theor Appl Genet 96:743–750

    Article  CAS  Google Scholar 

  • Dvorak J, McGuire PE, Cassidy B (1988) Apparent sources of the A genomes of wheats inferred from polymorphism in abundance and restriction fragment length of repeated nucleotide sequences. Genome 30:680–689

    CAS  Google Scholar 

  • Dvorak J, Diterlizzi P, Zhang HB, Resta P (1993) The evolution of polyploid wheats: identification of the A genome donor species. Genome 36:21–31

    Article  CAS  PubMed  Google Scholar 

  • Dvorak J, Luo MC, Yang ZL, Zhang H (1998) The structure of the Aegilops tauschii genepool and the evolution of hexaploid wheat. Theor Appl Genet 97:657–670

    Article  CAS  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using PHRED. II. Error probabilities. Genome Res 8:186–194

    CAS  PubMed  Google Scholar 

  • Gao SC, Gu YQ, Wu JJ, Coleman-Derr D, Huo NX, Crossman C, Jia JZ, Zuo Z, Ren ZL, Anderson OD, Kong XY (2007) Rapid evolution and complex structural organization in genomic regions harboring multiple prolamin genes in the polyploid wheat genome. Plant Mol Biol 65:189–203

    Article  CAS  PubMed  Google Scholar 

  • Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms—synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene Rbcl. Proc Natl Acad Sci 93:10274–10279

    Article  CAS  PubMed  Google Scholar 

  • Giles RJ, Brown TA (2006) GluDy allele variation in Aegilops tauschii and Triticum aestivum: implications for the origins of hexaploid wheats. Theor Appl Genet 112:1563–1572

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gu YG, Salse J, Coleman-Derr D, Dupin A, Crossman C, Lazo GR, Huo N, Belcram H, Ravel C, Charmet G, Charles M, Anderson B, Chalhoub B (2006) Types and rates of sequence evolution at the high-molecular weight glutenin locus in hexaploid wheat and its ancestral genomes. Genetics 174:1493–1504

    Article  CAS  PubMed  Google Scholar 

  • Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527

    Article  CAS  PubMed  Google Scholar 

  • Huang XQ, Cloutier S (2007) Hemi-nested touchdown PCR combined with primer-template mismatch PCR for rapid isolation and sequencing of low molecular weight glutenin subunit gene family from a hexaploid wheat BAC library. BMC Genetics 8:18

    Article  CAS  PubMed  Google Scholar 

  • Huang XQ, Cloutier S (2008) Molecular characterization and genomic organization of low molecular weight glutenin subunit genes at the Glu-3 loci in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 116:953–966

    Article  CAS  PubMed  Google Scholar 

  • Huang XQ, Röder MS (2004) Molecular mapping of powdery mildew resistance genes in wheat: a review. Euphytica 137:203–223

    Article  CAS  Google Scholar 

  • Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci 99:8133–8138

    Article  CAS  PubMed  Google Scholar 

  • Huang XQ, Hsam SLK, Mohler V, Röder MS, Zeller FJ (2004) Genetic mapping of three alleles at the Pm3 locus conferring powdery mildew resistance in common wheat (Triticum aestivum L.). Genome 47:1130–1136

    Article  CAS  PubMed  Google Scholar 

  • Huang XQ, Cloutier S, Lycar L, Radovanovic N, Humphreys DG, Noll JS, Somers DJ, Brown PD (2006) Molecular detection of QTLs for agronomic and quality traits in a doubled haploid population derived from two Canadian wheats (Triticum aestivum L.). Theor Appl Genet 113:753–766

    Article  CAS  PubMed  Google Scholar 

  • Huo N, Vogel JP, Lazo GR, You FM, Ma Y, McMahon S, Dvorak J, Anderson OD, Luo MC, Gu YQ (2009) Structural characterization of Brachypodium genome and its syntenic relationship with rice and wheat. Plant Mol Biol 70:47–61

    Article  CAS  PubMed  Google Scholar 

  • Isidore E, Scherrer B, Chalhoub B, Feuillet C, Keller B (2005) Ancient haplotypes resulting from extensive rearrangements in the wheat A genome have been maintained in species of three different ploidy levels. Genome Res 15:526–536

    Article  CAS  PubMed  Google Scholar 

  • Johal J, Gianibelli MC, Rahman S, Morell MK, Gale KR (2004) Characterization of low-molecular-weight glutenin genes in Aegilops tauschii. Theor Appl Genet 109:1028–1040

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kronmiller BA, Wise RP (2008) TEnest: automated chronological annotation and visualization of nested plant transposable elements. Plant Physiol 146:45–49

    Article  CAS  PubMed  Google Scholar 

  • Li XH, Ma WJ, Gao LY, Zhang YZ, Wang AL, Ji KM, Wang K, Appels R, Yan YM (2008) A novel chimeric low-molecular-weight glutenin subunit gene from the wild relatives of wheat Aegilops kotschyi and Ae. juvenalis: evolution at the Glu-3 loci. Genetics 180:93–101

    Article  CAS  PubMed  Google Scholar 

  • McCartney CA, Somers DJ, Lukow O, Ames N, Noll J, Cloutier S, Humphreys DG, McCallum BD (2006) QTL analysis of quality traits in the spring wheat cross RL4452 × AC Domain. Plant Breed 125:565–575

    Article  CAS  Google Scholar 

  • Nilmalgoda S, Cloutier S, Walichnowski AZ (2003) Construction and characterization of a bacterial artificial chromosome (BAC) library of hexaploid wheat (Triticum aestivum L) and validation of genome coverage using locus-specific primers. Genome 46:870–878

    Article  CAS  PubMed  Google Scholar 

  • Özdemir N, Cloutier S (2005) Expression analysis and physical mapping of low-molecular-weight glutenin loci in hexaploid wheat (Triticum aestivum L.). Genome 48:401–411

    Article  PubMed  Google Scholar 

  • Ragupathy R, Cloutier S (2008) Genome organisation and retrotransposon driven molecular evolution of the endosperm Hardness (Ha) locus in Triticum aestivum cv. Glenlea. Mol Gen Genomics 116:283–296

    CAS  Google Scholar 

  • Sabelli P, Shewry PR (1991) Characterization and organization of gene families at the Gli-1 loci of bread and durum wheat by restriction fragment analysis. Theor Appl Genet 83:209–216

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • SanMiguel PJ, RamaKrishna W, Bennetzen JL, Busso C, Dubovsky J (2002) Transposable elements, genes and recombination in a 215-kb contig from wheat chromosome 5A(m). Funct Integr Genomics 2:70–80

    Article  CAS  PubMed  Google Scholar 

  • Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958

    Article  CAS  PubMed  Google Scholar 

  • Srichumpa P, Brunner S, Keller B, Yahiaoui N (2005) Allelic series of four powdery mildew resistance genes at the Pm3 locus in hexaploid bread wheat. Plant Physiol 139:885–895

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599 (Publication PDF at http://www.kumarlab.net/publications)

    Article  CAS  PubMed  Google Scholar 

  • Tommasini L, Yahiaoui N, Srichumpa P, Keller B (2006) Development of functional markers specific for seven Pm3 resistance alleles and their validation in the bread wheat gene pool. Theor Appl Genet 114:165–175

    Article  CAS  PubMed  Google Scholar 

  • Veraverbeke WS, Delcour JA (2002) Wheat protein composition and properties of wheat glutenin in relation to breadmaking functionality. Crit Rev Food Sci Nutri 42:179–208

    Article  CAS  Google Scholar 

  • Vitte C, Ishii T, Lamy F, Brar DS, Panaud O (2004) Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.). Mol Gen Genomics 272:504–511

    Article  CAS  Google Scholar 

  • Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54–61

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yahiaoui N, Srichumpa P, Dudler R, Keller B (2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J 37:528–538

    Article  CAS  PubMed  Google Scholar 

  • Yahiaoui N, Brunner S, Keller B (2006) Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J 47:85–98

    Article  CAS  PubMed  Google Scholar 

  • Yahiaoui N, Kaur N, Keller B (2009) Independent evolution of functional Pm3 resistance genes in wild tetraploid wheat and domesticated bread wheat. Plant J 57:846–856

    Article  CAS  PubMed  Google Scholar 

  • Zeller FJ, Hsam SLK (1998) Progress in breeding for resistance to powdery mildew in common wheat (Triticum aestivum L.). In: Slinkard AE (ed) Proceedings of the Ninth International Wheat Genetics Symposium, vol. 1. University Extension Press, University of Saskatchewan, Saskatoon, pp 178–180

    Google Scholar 

  • Zhang W, Gianibelli MC, Rampling LR, Gale KR (2004) Characterisation and marker development for low molecular weight glutenin genes from Glu-A3 alleles of bread wheat (Triticum aestivum L.). Theor Appl Genet 108:1409–1419

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are very grateful to Mike Shillinglaw for preparation of the figures and Joanne Schiavoni for manuscript preparation. We thank Andrzej Walichnowski for critical reading of this manuscript. This project was supported by the Canadian Crop Genomics Initiative of Agriculture and Agri-Food Canada. This is Agriculture and Agri-Food Canada contribution # 1973.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sylvie Cloutier.

Additional information

Zi-Ning Wang and Xiu-Qiang Huang contributed equally to this manuscript.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. 1S

(Supplementary data) Deduced amino acid sequence alignment of the known PM3 isotypes with PM3-like from the TaBAC133L16 of the Glenlea B genome shows conservation of sequence blocks (boxes). (GIF 233 kb)

High Resolution Image (TIFF 879 kb)

Fig. 1S

(Supplementary data) Deduced amino acid sequence alignment of the known PM3 isotypes with PM3 like from the TaBAC133L16 of the Glenlea B genome shows conservation of sequence blocks (boxes). (GIF 219 kb)

High Resolution Image (TIFF 857 kb)

Fig. 2S

(Supplementary data) Comparison of BAC sequences by dot plot analysis performed using the JDOTTER program (Brodie et al. 2004) with default parameters. A Comparison of the two A genome sequences from T. turgidum and T. aestivum. B Comparison of the two B genome sequences from T. turgidum and T. aestivum. C Comparison of the A and B genome sequences from T. aestivum. (GIF 326 kb)

High Resolution Image (TIFF 4853 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, ZN., Huang, XQ. & Cloutier, S. Recruitment of closely linked genes for divergent functions: the seed storage protein (Glu-3) and powdery mildew (Pm3) genes in wheat (Triticum aestivum L.). Funct Integr Genomics 10, 241–251 (2010). https://doi.org/10.1007/s10142-009-0150-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-009-0150-y

Keywords

Navigation