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The PDI genes of wheat and their syntenic relationship to the esp2 locus of rice

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Abstract

The storage protein polymers in the endosperm, stabilised by disulphide bonds, determine a number of processing qualities of wheat dough. The enzyme protein disulphide isomerase (PDI), involved in the formation of disulphide bonds, is strongly suggested to play a role in the formation of wheat storage protein bodies. Reports of the rice mutant esp2 exhibiting aberrant storage protein deposition in conjunction with a lack of PDI expression provided strong indications of a direct role for PDI in storage protein deposition. The potential significance of wheat PDI prompted the present studies into exploring any orthology between wheat PDI genes and rice PDI and esp2 loci. By designing allele-specific (AS)-polymerase chain reaction (PCR) markers, two of the three wheat PDI genes could be genetically mapped to group 4 chromosomes and showed close association with GERMIN genes. Physical mapping led to localisation of wheat PDI genes to chromosomal “bins” on the proximal section of chromosome 4AL and distal sections of 4BS and 4DS. Identification of the putative PDI gene of rice and its comparison to the esp2 locus revealed that they were present at similar positions on the short arm of chromosome 11. Analysis of a large section of the PDI-containing section of rice chromosome 11S revealed a number of putative orthologues from The Institute for Genomic Research Triticum aestivum Gene Index database, of which five had been mapped, each localising to group 4 chromosomes, many in good agreement with our mapping results. The results strongly suggest a close linkage between the esp2 marker and the PDI gene of rice and an orthology between the PDI loci of rice and wheat and predict quantitative-trait loci involved in storage protein deposition at the PDI loci.

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Abbreviations

AS:

allele specific

BAC:

bacterial artificial chromosome

cDNA:

complementary DNA

DH:

doubled haploid

DPA:

days post-anthesis

ER:

endoplasmic reticulum

EST:

expressed sequence tag

gDNA:

genomic DNA

PCR:

polymerase chain reaction

PDI:

protein disulfide isomerase

QTL:

quantitative trait loci

RFLP:

restriction fragment length polymorphism

SNP:

single nucleotide polymorphism

References

  • Bailey PC, McKibbin RS, Lenton JR, Holdsworth MJ, Flintham JE, Gale MD (1999) Genetic map locations for orthologous Vp1 genes in wheat and rice. Theor Appl Genet 98:281–284

    Article  CAS  Google Scholar 

  • Berna A, Bernier F (1999) Regulation by biotic and abiotic stress of a wheat germin gene encoding oxalate oxidase, a H2O2-producing enzyme. Plant Mol Biol 39:539–549

    Article  PubMed  CAS  Google Scholar 

  • Bryan GJ, Stephenson P, Collins A, Kirby J, Smith JB, Gale MD (1999) Low levels of DNA sequence variation among adapted genotypes of hexaploid wheat. Theor Appl Genet 99:192–198

    Article  CAS  Google Scholar 

  • Bulleid NJ, Freedman RB (1988) Defective co-translational formation of disulphide bonds in protein disulphide-isomerase-deficient microsomes. Nature 335:649–651

    Article  PubMed  CAS  Google Scholar 

  • Caliskan M, Cuming AC (1998) Spatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination. Plant J 15:165–171

    Article  PubMed  CAS  Google Scholar 

  • Chalmers KJ, Campbell AW, Kretschmer J, Karakousis A, Henschke PH, Pierens S, Harker N, Pallotta M, Cornish GB, Shariflou MR, Rampling LR, McLauchlan A, Daggard G, Sharp PJ, Holton TA, Sutherland MW, Appels R, Langridge P (2001) Construction of three linkage maps in bread wheat, Triticum aestivum. Aust J Agric Res 52:1089–1119

    Article  CAS  Google Scholar 

  • Ciaffi M, Dominici L, Tanzarella OA, Porceddu E (1999) Chromosomal assignment of gene sequences coding for protein disulphide isomerase (PDI) in wheat. Theor Appl Genet 98:405–410

    Article  CAS  Google Scholar 

  • Ciaffi M, Paolacci AR, Dominici L, Tanzarella OA, Porceddu E (2001) Molecular characterization of gene sequences coding for protein disulfide isomerase (PDI) in durum wheat (Triticum turgidum ssp durum). Gene 265:147–156

    Article  PubMed  CAS  Google Scholar 

  • DuPont FM, Hurkman WJ, Tanaka CK, Chan R (1998) BiP, HSP70, NDK and PDI in wheat endosperm. I. Accumulation of mRNA and protein during grain development. Physiol Plant 103:70–79

    Article  CAS  Google Scholar 

  • Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Heredity 87:295–307

    CAS  Google Scholar 

  • Ferrari DM, Soling HD (1999) The protein disulphide-isomerase family: unravelling a string of folds. Biochem J 339:1–10

    Article  PubMed  CAS  Google Scholar 

  • Freedman RB, Hirst TR, Tuite MF (1994) Protein disulphide isomerase—building bridges in protein folding. Trends Biochem Sci 19:331–336

    Article  PubMed  CAS  Google Scholar 

  • Grimwade B, Tatham AS, Freedman RB, Shewry PR, Napier JA (1996) Comparison of the expression patterns of genes coding for wheat gluten proteins and proteins involved in the secretory pathway in developing caryopses of wheat. Plant Mol Biol 30:1067–1073

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harker N, Rampling LR, Shariflou MR, Hayden MJ, Holton TA, Morell MK, Sharp PJ, Henry RJ, Edwards KJ (2001) Microsatellites as markers for Australian wheat improvement. Aust J Agric Res 52:1121–1130

    Article  CAS  Google Scholar 

  • Johnson JC, Bhave M (2004) Molecular characterisation of the protein disulphide isomerase genes of wheat. Plant Sci 167:397–410

    Article  CAS  Google Scholar 

  • Johnson JC, Clarke BC, Bhave M (2001) Isolation and characterisation of cDNAs encoding protein disulphide isomerases and cyclophilins in wheat. J Cereal Sci 34:159–171

    Article  CAS  Google Scholar 

  • Kammholz SJ, Campbell AW, Sutherland MW, Hollamby GJ, Martin PJ, Eastwood RF, Barclay I, Wilson RE, Brennan PS, Sheppard JA (2001) Establishment and characterisation of wheat genetic mapping populations. Aust J Agric Res 52:1079–1088

    Article  CAS  Google Scholar 

  • Kumamaru T, Satoh H, Iwata N, Omura T, Ogawa M (1987) Mutants for rice storage proteins 3: genetic analysis of mutants for storage proteins of protein bodies in the starchy endosperm. Jpn J Genet 62:333–339

    Article  Google Scholar 

  • Lane BG (2002) Oxalate, germins, and higher-plant pathogens. IUBMB Life 53:67–75

    PubMed  CAS  Google Scholar 

  • Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993) Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 268:12239–12242

    PubMed  CAS  Google Scholar 

  • La Rota M, Sorrells ME (2004) Comparative DNA sequence analysis of mapped wheat ESTs reveals the complexity of genome relationships between rice and wheat. Funct Integr Genomics 4:34–46

    Article  PubMed  CAS  Google Scholar 

  • Liu R, Olsen OA, Kreis M, Halford NG (1992) Molecular cloning of a novel barley seed protein gene that is repressed by abscisic acid. Plant Mol Biol 18:1195–1198

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Appels R, Bekes F, Larroque O, Morell MK, Gale KR. Genetic characterisation of dough rheological properties in a wheat doubled haploid population: additive genetic effects and epistatic interactions. Theor Appl Genet (in Press). Available online; DOI:10.1007/s00122-005-2001-0

  • Manly K, Olson J (1999) Overview of QTL mapping software and introduction to Map Manager QT. Mamm Genome 10:327–334

    Article  PubMed  CAS  Google Scholar 

  • Marino CL, Nelson JC, Lu YH, Sorrells ME, Leroy P, Tuleen NA, Lopes CR, Hart GE (1996) Molecular genetic maps of the group 6 chromosomes of hexaploid wheat (Triticum aestivum L. em. Thell). Genome 39:359–366

    CAS  PubMed  Google Scholar 

  • Miftahudin, Ross K, Ma X-F, Mahmoud AA, Layton J, Rodriguez Milla MA, Chikmawati T, Ramalingam J, Feril O, Pathan MS, Surlan Momirovic G, Kim S, Chema K, Fang P, Haule L, Struxness H, Birkes J, Yaghoubian C, Skinner R, McAllister J, Nguyen V, Qi LL, Echalier B, Gill BS, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvorák J, Dilbirligi M, Gill KS, Peng JH, Lapitan NLV, Bermudez-Kandianis CE, Sorrells ME, Hossain KG, Kalavacharla V, Kianian SF, Lazo GR, Chao S, Anderson OD, Gonzalez-Hernandez J, Conley EJ, Anderson JA, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Nguyen HT, Gustafson JP (2004) Analysis of expressed sequence tag loci on wheat chromosome group 4. Genetics 168:651–663

    Article  PubMed  CAS  Google Scholar 

  • Orsi A, Sparvoli F, Ceriotti A (2001) Role of individual disulfide bonds in the structural maturation of a low molecular weight glutenin subunit. J Biol Chem 276:32322–32329

    Article  PubMed  CAS  Google Scholar 

  • Patnaik D, Khurana P (2001) Germins and germin like proteins: an overview. Indian J Exp Biol 39:191–200

    PubMed  CAS  Google Scholar 

  • Pestova E, Ganal MW, Röder MS (2000) Isolation and mapping of microsatellite markers specific for the D genome of bread wheat. Genome 43:689–697

    Article  PubMed  Google Scholar 

  • Roden LT, Miflin BJ, Freedman RB (1982) Protein disulphide-isomerase is located in the endoplasmic reticulum of developing wheat endosperm. FEBS Lett 38:121–124

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Sarma RN, Gill BS, Sasaki T, Galiba G, Sutka J, Laurie DA, Snape JW (1998) Comparative mapping of the wheat chromosome 5A Vrn-A1 region with rice and its relationship to QTL for flowering time. Theor Appl Genet 97:103–109

    Article  CAS  Google Scholar 

  • Sears ER (1954) The aneuploids of common wheat. In: Research bulletin 572. University of Missouri College of Agriculture, Agriculture Experimental Station, Columbia, MO, pp 3–58

    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  PubMed  CAS  Google Scholar 

  • Shewry PR, Halford NG, Tatham AS, Popineau Y, Lafiandra D, Belton PS (2003) The high molecular weight subunits of wheat glutenin and their role in determining wheat processing properties. Adv Food Nutr Res 45:219–302

    Article  PubMed  CAS  Google Scholar 

  • Shimoni Y, Galili G (1996) Intramolecular disulfide bonds between conserved cysteines in wheat gliadins control their deposition into protein bodies. J Biol Chem 271:18869–18874

    Article  PubMed  CAS  Google Scholar 

  • Shimoni Y, Zhu X, Levanony H, Segal G, Galili G (1995) Purification, characterization, and intracellular localization of glycosylated protein disulfide isomerase from wheat grains. Plant Physiol 108:327–335

    Article  PubMed  CAS  Google Scholar 

  • Singh NK, Raghuvanshi S, Srivastava SK, Gaur A, Pal AK, Dalal V, Singh A, Ghazi IA, Bhargav A, Yadav M, Dixit A, Batra K, Gaikwad K, Sharma TR, Mohanty A, Bharti AK, Kapur A, Gupta V, Kumar D, Vij S, Vydianathan R, Khurana P, Sharma S, McCombie WR, Messing J, Wing R, Sasaki T, Khurana P, Mohapatra T, Khurana JP, Tyagi AK (2004) Sequence analysis of the long arm of rice chromosome 11 for rice–wheat synteny. Funct Integr Genomics 4:102–117

    Article  PubMed  CAS  Google Scholar 

  • Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol 128:1212–1222

    Article  PubMed  CAS  Google Scholar 

  • Tarchini R, Biddle P, Wineland R, Tingey S, Rafalski A (2000) The complete sequence of 340 kb of DNA around the rice adh1-adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell 12:381–391

    Article  PubMed  CAS  Google Scholar 

  • Van den Berg B, Chung E, Robinson C, Mateo P, Dobson C (1999) The oxidative refolding of hen lysozyme and its catalysis by protein disulfide isomerase. EMBO J 18:4794–4803

    Article  PubMed  Google Scholar 

  • Ware D, Jaiswal P, Ni J, Pan X, Chang K, Clark K, Teytelman L, Schmidt S, Zhao W, Cartinhour S, McCouch S, Stein L (2002) Gramene: a resource for comparative grass genomics. Theor Appl Genet 30:103–105

    CAS  Google Scholar 

  • Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J, Fujii F, Shomura A, Ando T, Kono I, Waki K, Yamamoto K, Yano M, Matsumoto T, Sasaki T (2002) A comprehensive rice transcript map containing 6591 expressed sequence tag sites. Plant Cell 14:525–535

    Article  PubMed  CAS  Google Scholar 

  • Yao Y, Zhou Y, Wang C (1997) Both the isomerase and chaperone activities of protein disulfide isomerase are required for the reactivation of reduced and denatured acidic phospholipase A2. EMBO J 16:651–658

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors would like to express their gratitude to Dr. Bryan Clarke for extending the use of lab facilities at CSIRO-Plant Industry (Canberra) for conducting part of this research and providing general advice for it, and Lynette Rampling at CSIRO Plant Industry for technical assistance during this work. This work was funded by a Grains Industry Research Ph.D. scholarship from the Grains Research and Development Corporation (GRDC) to J.J.

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Authors and Affiliations

  1. School of Molecular Sciences, Victoria University, P.O. Box 14428, Melbourne, Victoria, MC 8001, Australia

    Joshua C. Johnson

  2. Molecular Plant Breeding CRC, Murdoch University, Murdoch, WA, 6150, Australia

    Rudi Appels

  3. Department of Agriculture Western Australia, Murdoch, WA, 6150, Australia

    Rudi Appels

  4. Environment and Biotechnology Centre, Faculty of Life and Social Sciences, Swinburne University of Technology, P.O. Box 218, Hawthorn, Victoria, 3122, Australia

    Mrinal Bhave

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  1. Joshua C. Johnson
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Correspondence to Mrinal Bhave.

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Johnson, J.C., Appels, R. & Bhave, M. The PDI genes of wheat and their syntenic relationship to the esp2 locus of rice. Funct Integr Genomics 6, 104–121 (2006). https://doi.org/10.1007/s10142-005-0003-2

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  • DOI: https://doi.org/10.1007/s10142-005-0003-2

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