Skip to main content
SpringerLink
Log in

Genetic and in silico comparative mapping of the polyphenol oxidase gene in bread wheat (Triticum aestivum L.)

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

Abstract

Polyphenol oxidases (PPOs) are involved in the time-dependent darkening and discolouration of Asian noodles and other wheat end products. In this study, a doubled haploid (DH) population derived from Chara (moderately high PPO activity)/WW2449 (low PPO activity) was screened for PPO activity based on l-DOPA and l-tyrosine assays using whole seeds. Both these assays were significantly genetically correlated (r=0.91) in measuring the PPO activity in this DH population. Quantitative trait loci (QTLs) analysis utilising a skeleton map enabled us to identify a major QTL controlling PPO activity based on l-DOPA and l-tyrosine on the long arm of chromosome 2A. The simple sequence repeat (SSR) marker GWM294b explained over 82% of the line mean phenotypic variation from samples collected in both 2000 and 2003. Four SSR markers were validated for PPO linkage in genetically diverse backgrounds and proven to correctly predict the PPO activity in more than 92% of wheat lines. Physical mapping using deletion lines of Chinese Spring has confirmed the location of the GWM294b, GWM312 and WMC170 on chromosome 2AL, between deletion breakpoints 2AL-C to 0.85. In order to identify functional gene markers, data searches for alignments between rice BAC/PAC clones assembled on chromosome 1 and 4, chromosome 7, and (1) the wheat expressed sequence tags mapped in deletion bin (2AL-C to 0.85) and (2) the coding sequence of a previously cloned wheat PPO gene were made and found significant sequence similarities with the PPO gene or common central domain of tyrosinase. Available PPO gene sequences in the National Centre for Biotechnology Information (NCBI) database have revealed that there is a significant molecular diversity at the nucleotide and amino acid level in the wheat PPO genes.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

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  CAS  PubMed  Google Scholar 

  • Anderson JV (2003) Characterization of a wheat polyphenol oxidase (PPO) expressed predominately in developing grain. NCBI database (AY515506)

  • Anderson JV, Morris CF (2001) An improved whole-seed assay for screening wheat germplasm for polyphenol oxidase activity. Crop Sci 41:1697–1705

    CAS  Google Scholar 

  • Baik BK, Czuchajowsa Z, Pomeranz Y (1994) Comparison of polyphenol oxidase activity in wheat and flours from Australian and US cultivars. J Cereal Sci 19:291–296

    CAS  Google Scholar 

  • Baik BK, Czuchajowsa Z, Pomeranz Y (1995) Discolouration of dough for oriental noodles. Cereal Sci 72:198–205

    CAS  Google Scholar 

  • Bernier AM, Howes NK (1994) Quantification of variation in tyrosinase activity among durum and common wheat cultivars. J Cereal Sci 19:157–159

    CAS  Google Scholar 

  • Bertrand G, Muttermilch W (1907) Sur I’esistence d’une tyrosinase dans le son de fromet. C R Hebd Seances Acad Sci 144:1285

    CAS  Google Scholar 

  • Bhowal JG, Bannerjee SK, Joshi MG (1969) The evaluation of the phenol colour reaction gene in wheat. Jpn J Genet 44:123–128

    Google Scholar 

  • Box NF, Wyeth JR, Mayne CJ, O’Gorman LE, Martin NG, Sturm RA (1998) Complete sequence and polymorphism study of the human TYRP1 gene encoding tyrosinase related protein 1. Mamm Genome 9(1):50–53

    CAS  PubMed  Google Scholar 

  • Bucheli CS, Dry IB, Robinson SM (1998) Isolation of a full length cDNA encoding polyphenol oxidase from sugarcane, a C4 grass. Plant Mol Biol 31:1233–1238

    Google Scholar 

  • Cary JW, Lax AR, Flurkey WH (1992) Cloning and characterisation of cDNA coding for Vicia faba polyphenol oxidase. Plant Mol Biol 20:245–253

    CAS  PubMed  Google Scholar 

  • Cohen T, Muller RM, Tomita Y, Shibahara S (1990) Nucleotide sequence of the cDNA encoding human tyrosinase-related protein. Nucleic Acids Res 18(9):2807–2808

    CAS  PubMed  Google Scholar 

  • Coombes NE (2002) The reactive tabu search for efficient correlated experimental designs. PhD thesis, Liverpool John Moores University, Liverpool UK

  • Crosbie GB, Solah VA, Chiu P, Lambe WJ (1996) Selection for improved colour stability in noodles. In: Wrigley CW (ed) Proceedings of the Australian Cereal Chemistry Conference 46th, Sydney, 4–6 Sept 1996. Royal Australian Chemist Institute, North Melbourne, Victoria, Australia, pp 120–122

    Google Scholar 

  • Dayhoff MR, Schwartz RM, Orcutt BC (1978) A model of evolutionary changes in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Springs, MD, pp 345–352

    Google Scholar 

  • Delaney DE, Nasuda S, Endo TR, Gill BS, Hulbert SH (1995) Cytologically based physical maps of the group 2 chromosomes of wheat. Theor Appl Genet 91:568–573

    CAS  Google Scholar 

  • Demeke T, Morris CF (2002) Molecular characterisation of wheat polyphenol oxidase (PPO). Theor Appl Genet 104:813–818

    Google Scholar 

  • Demeke T, Change HG, Morris CF (2001a) Effect of germination, seed abrasion and seed size on polyphenol oxidase assay activity in wheat. Plant Breed 120:369–373

    CAS  Google Scholar 

  • Demeke T, Morris CF, Campbell KG, King GE, Anderson JA, HG Chang (2001b) Wheat polyphenol oxidase: distribution and genetic mapping in three inbred line populations. Crop Sci 41:1750–1757

    CAS  Google Scholar 

  • Devos KM, Millan T, Gale MD (1993) Comparative RFLP maps of the homoeologous group-2 chromosomes of wheat, rye and barley. Theor Appl Genet 85:784–792

    Google Scholar 

  • Dexter JE, Preston KR, Matsuo RR, Tipples KH (1984) Development of a high extraction flour for the GRL Pilot Mill to evaluate Canadian wheat potential for the Chinese market. Can Inst Food Sci Technol 14:253–259

    Google Scholar 

  • Dry IB, Robinson SP (1994) Molecular cloning and characterisation of grape polyphenol oxidase. Plant Mol Biol 26(1):495–502

    CAS  PubMed  Google Scholar 

  • Eckermann PJ, Verbyla AP, Cullis BR, Thompson R (2001) The analysis of quantitative traits in wheat mapping populations. Aust J Agric Res 52:1195–1206

    CAS  Google Scholar 

  • Edwards RA, Ross AS, Mares DJ, Ellison FW, Tomlinson JD (1989) Enzymes from rain damaged and laboratory-germinated wheats. I. Effects on product quality. J Cereal Sci 10:157–167

    CAS  Google Scholar 

  • Faridi H (1988) Flat breads. In: Pomeranz Y (ed) Wheat chemistry and technology, vol 2, 3rd edn. American Association of Cereal Chemists, St Paul, MN, pp 457–506

    Google Scholar 

  • Feillet P, Autran JC, Icard-Verniere C (2000) Pasta brownness: an assessment. J Cereal Sci 32:215–233

    CAS  Google Scholar 

  • Felsenstein J (1995) PHYLIP: phylogeny interference package, ver 3.57c. University of Washington Press, Seattle

    Google Scholar 

  • Feng Q, Zhang Y, Hao P, Wang S, Fu G et al (2002) Sequence and analysis of rice chromosome 4. Nature 420(6913):316–320

    CAS  PubMed  Google Scholar 

  • Gajderowicz LJ (1979) Progress in the refrigerated dough industry. Cereal Foods World 24:44–45

    Google Scholar 

  • Gill KS, Gill BS, Endo TR, Taylor T (1996) Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics 144:1883–1891

    CAS  PubMed  Google Scholar 

  • Gilmour AR, Cullis BR, Welham SJ, Thompson R (2004) ASReml reference manual. Orange Agricultural Institute, NSW, Australia

    Google Scholar 

  • Guidet F, Rogowsky P, Taylor C, Song W, Langridge P (1991) Cloning and characterisation of a new rye specific repeated sequence. Genome 34:81–87

    Google Scholar 

  • Gupta PK, Balyan H, Edwards K, Isaac P, Korzun V et al (2002) Genetic mapping of 66 new microsatellite (SSR) loci in bread wheat. Theor Appl Genet 105:413–422

    Google Scholar 

  • Guyomar’h H, Soudille P, Charmet G, Edwards KJ, Bernard M (2002) Characterisation of polymorphic microsatellite markers from Aegilops taushii and transferability to the D genome of bread wheat. Theor Appl Genet 104:1164–1172

    Article  CAS  PubMed  Google Scholar 

  • Guyot R, Keller B (2004) Ancestral genome duplication in rice. Genome 47:610–614

    CAS  PubMed  Google Scholar 

  • Hatcher DW, Kruger JE (1993) Distribution of polyphenol oxidase in flour millstreams of Canadian common wheat classes milled to three extraction rates. Cereal Chem 70:51–55

    CAS  Google Scholar 

  • Hayden M, Good G, Sharp PJ (2002) Sequence tagged microsatellite profiling (STMP): improved isolation of DNA sequence flanking target SSRs. Nucleic Acids Res 30(23):129–133

    PubMed  Google Scholar 

  • Hind G, Marshak DR, Coughlan SJ (1995) Spinach thalakoid polyphenol oxidase: cloning, characterisation and relation to a putative protein kinase. Biochemistry 34(25):8157–8164

    CAS  PubMed  Google Scholar 

  • Jimenez M, Dubcovsky J (1999) Chromosome location of genes affecting polyphenol oxidase activity in seeds of common and durum wheat. Plant Breed 118:395–398

    CAS  Google Scholar 

  • John JA, Williams ER (1995) Cyclic and computer generated designs. Chapman and Hall, London

    Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Jukanti AK, Bruckner PL, Fischer AM (2004a) Evaluation of wheat polyphenol oxidase genes. NCBI database (Locus AY596266)

  • Jukanti AK, Bruckner PL, Fischer AM (2004b) Evaluation of wheat polyphenol oxidase genes. NCBI (Locus AY596267)

  • Jukanti AK, Bruckner PL, Fischer AM (2004c) Evaluation of wheat polyphenol oxidase genes. NCBI database (Locus AY596268)

  • Jukanti AK, Bruckner PL, Fischer AM (2004d) Evaluation of wheat polyphenol oxidase genes. NCBI database (Locus AY596269)

  • Jukanti AK, Bruckner PL, Fischer AM (2004e) Evaluation of wheat polyphenol oxidase genes. NCBI database (Locus AY596270)

  • Kosambi DD (1944) The estimation of map distances from recombination values. Annu Eugen 12:172–175

    Google Scholar 

  • Kruger JE (1976) Changes in the polyphenol oxidases of wheat during kernel growth and maturation. Cereal Chem 53:201–213

    CAS  Google Scholar 

  • Kruger JE, Matsuo RR, Preston K (1992) A comparison of methods for the prediction of Cantonese noodle colour. Can J Plant Sci 72:1021–1029

    Google Scholar 

  • Kruger JE, Hatcher DW, DePauw R (1994a) A whole seed for polyphenol oxidase in Canadian prairie spring wheats and its usefulness as a measure of noodle darkening. Cereal Chem 71:324–326

    CAS  Google Scholar 

  • Kruger JE, Anderson MH, Dexter JE (1994b) Effect of flour refinement on raw Cantonese noodle colour and texture. Cereal Chem 71:177–182

    CAS  Google Scholar 

  • Kupper U, Niedermann DM, Travaglini G, Lerch K (1989) Isolation and characterisation of the tyrosinase gene from Neurospora crassa. J Biol Chem 264:17250–17258

    CAS  PubMed  Google Scholar 

  • Lang WH, van Holde KE (1991) Cloning and sequencing of Octopus deleini hemocyanin cDNA; derived sequences of functional units ode and odf. Proc Natl Acad Sci U S A 88:244–248

    CAS  PubMed  Google Scholar 

  • Li WL, Faris JD, Chittoor JM, Leach JE, Hulbert SH et al (1999) Genomic mapping of defense response genes in wheat. Theor Appl Genet 98:226–233

    Article  CAS  Google Scholar 

  • Ma XF, Ross K, Gustafson JP (2001) Physical mapping of restriction fragment length polymorphism (RFLP) markers in homoeologous groups 1 and 3 chromosomes of wheat by in situ hybridisation. Genome 44:401–412

    Article  CAS  PubMed  Google Scholar 

  • Mahoney RR, Ramsay M (1992) A rapid tyrosinase test for detecting contamination of durum wheat. J Cereal Sci 15:267–270

    CAS  Google Scholar 

  • Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932

    Article  CAS  PubMed  Google Scholar 

  • Mares DJ, Campbell AW (2001) Mapping component of flour and noodle colour in Australian wheat. Aust J Agric Res 52:1297–1309

    Article  CAS  Google Scholar 

  • Mares DJ, Panozzo JF (1999) Impact of selection for low grain polyphenol oxidase activity on darkening in Asian noodles. In: Williamson P, Banks P, Haak I, Thompson J, Campbell A (eds) Proceedings of the 9th Assembly Wheat Breeding Society of Australia, pp 32–33

  • McCaig TN, Fenn DYK, Knox RE, DePauw RM, Clarke JM, McLeod JG (1999) Measuring polyphenol oxidase activity in a wheat breeding program. Can J Plant Sci 79:507–514

    CAS  Google Scholar 

  • McCallum JA, Walker JRL (1990) o-Diphenol oxidase activity, phenolic content and colour of new Zealand wheats, flours and milling streams. J Cereal Sci 12:83–96

    CAS  Google Scholar 

  • Mickelson-Young L, Endo TR, Gill BS (1995) A cytogenetic ladder-map of the wheat homoeologous group-4 chromosomes. Theor Appl Genet 90:1007–1011

    Google Scholar 

  • Milner M, Gould MR (1951) The quantitative determination of phenol oxidase activity in wheat varieties. Cereal Chem 28:473–478

    CAS  Google Scholar 

  • Miskelly DM (1981) Quality requirement for manufacture of fresh and instant Chinese noodles. In: Proceedings of the 31st Australian Cereal Chemistry Conference. Royal Australian Chemical Institute, Melbourne, Victoria, Australia, pp 61–62

    Google Scholar 

  • Morris CF, Anderson JV, Bettge AD, Sorrell ME (1998) Distribution of PPO activity among a large number of hexaploid wheat genotypes using an improved l-DOPA assay. Cereal Foods World 43:518

    Google Scholar 

  • Nelson JC, van Deynze AE, Autrique E, Sorrells ME, Lu YH et al (1995) Molecular mapping of wheat, homologous group 2. Genome 38:516–524

    CAS  Google Scholar 

  • Newman SM, Eannetta NT, Yu H, Prince JP, de Vicente MC et al (1993) Organisation of the tomato polyphenol oxidase gene family. Plant Mol Biol 21(6):1035–1051

    CAS  PubMed  Google Scholar 

  • Park WJ, Shelton DR, Ptereson CJ, Martin TJ, Kachman SD, Wehling RL (1997) Variation in polyphenol oxidase activity and quality characteristics among hard white wheat and hard red winter wheat samples. Cereal Chem 74:7–11

    CAS  Google Scholar 

  • Purdy LH, Loegering WQ, Konzak CF, Peterson CJ, Allen RE (1969) A proposed standard method for illustrating pedigrees of small grain varieties. Crop Sci 8:405–406

    Google Scholar 

  • Raman H, Karakousis A, Moroni JS, Raman R, Read BJ et al (2003) Development and allele diversity of microsatellite markers linked to the aluminium tolerance gene Alp in barley. Aust J Agric Res 54:1315–1321

    CAS  Google Scholar 

  • Rampling LR, Harker N, Shariflou MR, Morell MK (2001) Detection and analysis systems for microsatellite markers in wheat. Aust J Agric Res 52:1131–1141

    Article  CAS  Google Scholar 

  • Rani KU, Rao P, Leelavathi JS, Rao HP (2001) Distribution of enzymes in wheat flour mill streams. J Cereal Sci 34:233–242

    CAS  Google Scholar 

  • Röder MS, Korzun V, Gill BS, Ganal MW (1998a) The physical mapping of microsatellite markers in wheat. Genome 41:278–283

    Article  Google Scholar 

  • Röder MS, Korzum V, Wendehake K, Plaschke J, Tixier M-H, Leroy P, Ganal MW (1998b) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The number of nucleotides required to determine the branching order of three species, with special reference to the human–chimpanze–gorilla divergence. J Mol Evol 24:189–204

    Google Scholar 

  • Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316

    CAS  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    CAS  PubMed  Google Scholar 

  • Simone R, Pasqualone A, Clodoveo LM, Blanco A (2002) Genetic mapping of polyphenol oxidase in tetraploid wheat. Cell Mol Biol Lett 7:763–769

    PubMed  Google Scholar 

  • Singh R, Sheoran IS (1972) Enzymatic browning of whole wheat meal flour. J Sci Food Agric 23:121–125

    CAS  PubMed  Google Scholar 

  • Smith AB, Cullis BR, Appels R, Campbell AW, Cornish GB et al (2001) The statistical analysis of quality traits in plant improvement programs with application to the mapping of milling yields in wheat. Aust J Agric Res 52:1207–1219

    CAS  Google Scholar 

  • Sorrells ME, Rota ML, Bermudez-Kandianis CE, Greene RA, Kantety R et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827

    CAS  PubMed  Google Scholar 

  • Sourdille P, Singh S, Cadalen T, Brown-Guedira Gina L, Gay G et al (2004) Microsatellite-based deletion bin system for the establishment of genetic–physical map relationship in wheat Triticum aestivum L. Funct Integr Genomics 4:12–25

    CAS  PubMed  Google Scholar 

  • Souza E, Windes J, Udall J (1998) Inheritance of polyphenol oxidase reaction in three recombinant inbred populations of wheat. American Society of Agronomy, Madison, WI. Abstract 67

    Google Scholar 

  • Steffens JC, Harel E, Hunt MD (1994) Polyphenol oxidase. In: Ellis BE, Kuroki GW, Stafford HA (eds) Genetic engineering of plant secondary metabolism. Plenum, New York, pp 275–311

    Google Scholar 

  • Stephenson P, Bryan G, Kirby J, Collins A, Devos KM et al (1998) Fifty new microsatellite loci for the wheat genetic map. Theor Appl Genet 97:946–949

    Article  CAS  Google Scholar 

  • Sullivan B (1946) Oxidizing enzyme systems of wheat and flour. In: Anderson JA (ed) Enzymes and their role in wheat technology. Interscience, New York, p 215

    Google Scholar 

  • Takase M, Miura I, Nakata A, Takeuchi T, Nishioka M (1992) Cloning and sequencing of the cDNA encoding tyrosinase of the Japanese pond frog, Rana nigromaculata. Gene 121:359–363

    CAS  PubMed  Google Scholar 

  • Taneja SR, Abrol YP, Sachar RC (1974) Modulation of o-diphenolase and monophenolase enzymes during wheat grain development. Cereal Chem 51:457–465

    CAS  Google Scholar 

  • Thipyapong P, Joel DM, Steffens JC (1997) Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiol 113:707–718

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    CAS  PubMed  Google Scholar 

  • Tingey SV, Wolters P, Powell W, Doaln M, Miao G-H et al (2003) NCBI database (Locus BT009357)

  • Udall J (1996) Important alleles for noodle quality in winter wheat as identified by molecular markers. MS thesis, University of Idaho, Aberdeen

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Heredity 93(1):77–78

    Article  CAS  Google Scholar 

  • Werner JE, Endo TR, Gill BS (1992) Towards a cytogenetically based physical map of the wheat genome. Proc Natl Acad Sci U S A 89:11307–11311

    CAS  PubMed  Google Scholar 

  • Wrigley CW (1976) Single seed identification of wheat varieties: use of grain hardness testing, electrophoretic analysis and a rapid test paper for phenol reaction. J Sci Food Agric 27:429–432

    CAS  Google Scholar 

  • Yokoyama K, Suzuki H, Yasumoto K, Tomita Y, Shibahara S (1994) Molecular cloning and functional analysis of a cDNA coding for human DOPA chrome tautomerase/tyrosinase-related protein-2. Biochem Biophys Acta 1217(3):317–321

    CAS  PubMed  Google Scholar 

  • Zhang H, Nasuda S, Endo TR (2000) Identification of AFLP markers on the satellite region of chromosome 1BS in wheat. Genome 43:729–735

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the NSW Agricultural Genomics Centre funded under the BioFirst Initiative of the NSW Government for supporting this research work and to Dr. B.S. Gill, Kansas State University, USA, for providing seeds of deletion lines of wheat.

Author information

Authors and Affiliations

  1. NSW Department of Plant Industries and NSW Agricultural Genomics Centre, Wagga Wagga Agricultural Institute, Wagga Wagga, 2650, NSW, Australia

    Rosy Raman, Harsh Raman, Katie Johnstone, Chris Lisle, Alison Smith, Peter Matin & Helen Allen

  2. NSW Department of Primary Industries, Wagga Wagga Agricultural Institute, Private Mail Bag, Wagga Wagga, 2650, Australia

    Harsh Raman

Authors
  1. Rosy Raman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Harsh Raman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katie Johnstone
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chris Lisle
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alison Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peter Matin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Helen Allen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harsh Raman.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Raman, R., Raman, H., Johnstone, K. et al. Genetic and in silico comparative mapping of the polyphenol oxidase gene in bread wheat (Triticum aestivum L.). Funct Integr Genomics 5, 185–200 (2005). https://doi.org/10.1007/s10142-005-0144-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-005-0144-3

Keywords

Search

Navigation