Evolutionary Relationship of Wheat Protein Disulphide Isomerase (PDI) Gene Promoter Sequence Based on Phylogenetic Analysis


Protein disulphide isomerase (PDI) is an oxidoreductase enzyme abundant in the endoplasmic reticulum (ER). In plants, PDIs have been shown to assist the folding and deposition of seed storage proteins during the biogenesis of protein bodies in the endosperm. Cloning and characterization of the complete set of genes encoding PDI and PDI like proteins in bread wheat (Triticum aestivum cv. Chinese Spring) and the comparison of their sequence, structure and expression with homologous genes from other plant species were reported in our previous publications. Promoter sequences of three homoeologous genes encoding typical PDI, located on chromosome group 4 of bread wheat, and PDI promoter sequence analysis of Triticum urartu, Aegilops speltoides and Aegilops tauschii had also been reported previously. In this study, we report the isolation and sequencing of a ~700 bp region, comprising ~600 bp of the putative promoter region and 88 bp of the first exon of the typical PDI gene, in five accessions each from Triticum urartu (AA), Aegilops speltoides (BB) and Aegilops tauschii (DD). Sequence analysis indicated large variation among sequences belonging to the different genomes, while close similarity was found within each species and with the corresponding homoeologous PDI sequences of Triticum aestivum cv. CS (AABBDD) resulting in an overall high conservation of the sequence conferring endosperm-specific expression.

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A. Prabhu Dhanapal, "Evolutionary Relationship of Wheat Protein Disulphide Isomerase (PDI) Gene Promoter Sequence Based on Phylogenetic Analysis," American Journal of Plant Sciences, Vol. 3 No. 3, 2012, pp. 373-380. doi: 10.4236/ajps.2012.33045.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] B. S. Gill, R. Appels, A. M. Botha-Oberholster, C. R. Buell, J. L. Bennetzen, B. Chalhoub, F. Chumley, J. Dvorák, M. Iwanaga, B. Keller, W. Li, W. R. McCombie, Y. Ogihara, F. Quetier and T. Sasaki, “A Workshop Report on Wheat Genome Sequencing: International Genome Research on Wheat Consortium,” Genetics, Vol. 168, No. 2, 2004, pp. 1087-1096.doi:10.1534/genetics.104.034769
[2] H. Kihara, “Uber Cytolosgische Studien bei Einigen Getreidearten. I. Spezies-Bastarde des Weizens Und Weizenmggen-Bastarde,” Botanical Magazine (Tokyo), Vol. 33, 1919, pp. 17-38.
[3] H. Kihara, “Cytologische und Genetische Studien bei Wichtigen Getreidearten mit Besonderer Rucksicht auf das Verhalten der Chromosomen und die Sterilit?t in den Bastarden,” Memoirs of the College of Science, Kyoto Imperial University, Vol. 8, 1924, pp. 1-200.
[4] K. Sax, “Sterility in Wheat Hybrids. II. Chromosome Behavior in Partially Sterile Hybrids,” Genetics, Vol. 7, No. 6, 1922, pp. 49-68.
[5] R. Morris and E. R. Sears, “The Cytogenetics of Wheat and Its Relatives,” In: K. S. Quisenberry and L. P. Reitz, Ed., Wheat and Wheat Improvement, American Society of Agronomy, Madison, 1967, pp. 19-87.
[6] B. R. Baum and L. G. Bailey, “The Origin of the A Genome Donor of Wheats (Triticum: Poaceae): A Perspective Based on the Sequence Variation of the 5S DNA Gene Units,” Genetic Resources and Crop Evolution, Vol. 51, No. 2, 2004, pp. 183-196. doi:10.1023/B:GRES.0000020861.96294.f4
[7] J. Dvorak, P. Tetizi, H. B. Zhang and P. Resta, “The Evolution of Polyploid Wheats: Identification of the A Genome Donor Species,” Genome, Vol. 36, No. 1, 1993, pp. 21-31.doi:10.1139/g93-004
[8] M. Feldman, “Origin of Cultivated Wheat,” In: A. P. Bonjean and W. J. Angus, Ed., The World Wheat Book: A History of Wheat Breeding, Intercept Ltd., London, 2001, pp. 3-56.
[9] J. Jiang and B. S. Gill, “Different Species-Specific Chromosome Translocations in Triticum timopheevi and Triticum turgidum Support the Diphyletic Origin of Polyploid Wheats,” Chromosome Research, Vol. 2, No. 1, 1994, pp. 59-64. doi:10.1007/BF01539455
[10] H. Kihara, “Discovery of the DD-Analyser, One of the Ancestors of Triticum vulgare,” Agricuture and Horticulture, Vol. 19, 1944, pp. 889-890.
[11] J. Dvorak, M. C. Luo and Z. L. Yang, “Genetic Evidence on the Origin of T. aestivum L.,” In: A. Damania, Ed., The Origins of Agriculture and the Domestication of Crop Plants in the Near East, ICARDA, Aleppo, 1998, pp. 235-251.
[12] S. Chao, W. Zhang, E. Akhunov, J. Sherman, Y. Ma, M. C. Luo and J. Dubcovsky, “Analysis of Gene-Derived SNP Marker Polymorphism in US Wheat (Triticum aestivum L.) Cultivars,” Molecular Breeding, Vol. 23, No. 1, 2009, pp. 23-33. doi:10.1007/s11032-008-9210-6
[13] P. R. Shewry, J. A. Napier and A. S. Tatham, “Seed Storage Proteins: Structure and Biosynthesis,” Plant Cell, Vol. 7, No. 7, 1995, pp. 945-956.
[14] M. Schwaller, B. Wilkinson and H. F. Gilbert, “Reduction-Reoxidation Cycles Contribute to Catalysis of Disulfide Isomerisation by Protein-Disulfide Isomerase,” Journal of Biological Chemistry, Vol. 278, No. 9, 2003, pp. 7154-7159.doi:10.1074/jbc.M211036200
[15] B. P. Tu and J. S. Weissman, “Oxidative Protein Folding in Eukaryotes: Mechanisms and Consequences,” Journal of Cell Biology, Vol. 164, No. 3, 2004, pp. 341-346. doi:10.1083/jcb.200311055
[16] D. M. Ferrari and H. D. Soling, “The Protein Disulphide-Isomerase Family: Unravelling a String of Folds,” Biochemistry Journal, Vol. 339, No. 1, 1999, pp. 1-10. doi:10.1042/0264-6021:3390001
[17] B. S. Shorrosh and R. A. Dixon, “Molecular Cloning of a Putative Plant Endomembrane Protein Resembling Vertebrate Protein Disulfide-Isomerase and a Phosphatidylinositol-Specific Phospholinase,” Proceedings of National Academy of the Sciences, Vol. 88, No. 23, 1991, pp. 10941-10945.
[18] F. Chen and P. M. Hayes, “Nucleotide Sequence and Developmental Expression of Duplicated Genes Encoding Protein Disulfide Isomerase in Barley (Hordeum vulgare L.),” Plant Physiology, Vol. 106, No. 4, 1994, pp. 1705-1706.doi:10.1104/pp.106.4.1705
[19] C. P. Li and B. A. Larkins, “Expression of Protein Disulfide Isomerase Is Elevated in the Endosperm of the Maize Floury-2 Mutant,” Plant Molecular Biology, Vol. 30, No. 5, 1996, pp. 873-882.doi:10.1007/BF00020800
[20] S. J. Coughlan, C. Hastings and R. J. Winfrey, “Molecular Characterization of Plant Endoplasmic Reticulum: Identification of Protein Disulfide-Isomerase as the Major Reticuloplasmin,” European Journal of Biochemistry, Vol. 235, No. 1-2, 1996, pp. 215-224. doi:10.1111/j.1432-1033.1996.00215.x
[21] K. Iwasaki, S. Kamauchi, H. Wadahama, M. Ishimoto, T. Kawada and R. Urade, “Molecular Cloning and Characterization of Soybean Protein Disulfide Isomerase Family Proteins with Non Classic Active Center Motifs,” FEBS Journal, Vol. 276, No. 15, 2009, pp. 4130-4141. doi:10.1111/j.1742-4658.2009.07123.x
[22] S. Kamauchi, H. Wadahama, K. Iwasaki, Y. Nakamoto, K. Nishizawa, M. Ishimoto, T. Kawada and R. Urade, “Molecular Cloning and Characterization of Two Soybean Protein Disulfide Isomerases as Molecular Chaperones for Seed Storage Proteins,” FEBS Journal, Vol. 275, No. 10, 2008, pp. 2644-2658. doi:10.1111/j.1742-4658.2008.06412.x
[23] H. Wadahama, S. Kamauchi, M. Ishimoto, T. Kawada and R. Urade, “Protein Disulfide Isomerase Family Proteins Involved in Soybean Protein Biogenesis,” FEBS Journal, Vol. 274, No. 3, 2007, pp. 687-703. doi:10.1111/j.1742-4658.2006.05613.x
[24] H. Wadahama, S. Kamauchi, Y. Nakamoto, K. Nishizawa, M. Ishimoto, T. Kawada and R. Urade, “A Novel Plant Protein Disulfide Isomerase Family Homologous to Animal P5: Molecular Cloning and Characterization as a Functional Protein for Folding of Soybean Seed Storage Proteins,” FEBS Journal, Vol. 275, No. 3, 2008, pp. 399-410. doi:10.1111/j.1742-4658.2007.06199.x
[25] M. Ciaffi, A. R. Paolacci, L. Dominici, O. A. Tanzarella and E. Porceddu, “Molecular Characterization of Gene Sequences Coding for Protein Disulfide Isomerase (PDI) in Durum Wheat (Triticum turgidum ssp. durum),” Gene, Vol. 265, No. 1-2, 2001, pp. 147-156. doi:10.1016/S0378-1119(01)00348-1
[26] Y. Shimoni, G. Segal, X. Zhu and G. Galili, “Nucleotide Sequence of a Wheat cDNA Encoding Protein Disulfide Isomerase,” Plant Physiology, Vol. 107, No. 1, 1995, pp. 281. doi:10.1104/pp.107.1.281
[27] N. L. Houston, C. Fan, Q. Y. Xiang, J. M. Schulze, R. Jung and R. S. Boston, “Phylogenetic Analyses Identify 10 Classes of the Protein Disulfide Isomerase Family in Plants, Including Single-Domain Protein Disulfide Isomerase-Related Proteins,” Plant Physiology, Vol. 137, No. 2, 2005, pp. 762-778. doi:10.1104/pp.104.056507
[28] E. d'Aloisio, A. R. Paolacci, A. P. Dhanapal, O. A. Tanzarella, E. Porceddu and M. Ciaffi, “The Protein Disulfide Isomerase Gene Family in Bread Wheat (T. aestivum L.),” BMC Plant Biology, Vol. 10, 2010, pp. 101. doi:10.1186/1471-2229-10-101
[29] M. Ciaffi, L. Dominici, O. A. Tanzarella and E. Porceddu, “Chromosomal Assignment of Gene Sequences Coding for protein Disulphide Isomerase (PDI) in Wheat,” Theoritical and Applied Genetics, Vol. 98, No. 3-4, 1999, pp. 405-410. doi:10.1007/s001220051086
[30] M. Ciaffi, L. Dominici, E. Umana, O. A. Tanzarella and E. Porceddu, “Restriction Fragment Length Polymorphism (RFLP) for Protein Disulfide Isomerase (PDI) Gene Sequences in Triticum and Aegilops Species,” Theoritical and Applied Genetics, Vol. 98, No. 1-2, 2000, pp. 220-226. doi:10.1007/s001220051472
[31] M. Ciaffi, A. R. Paolacci, E. d'Aloisio, O. A. Tanzarella and E. Porceddu, “Cloning and Characterization of Wheat PDI (Protein Disulfide Isomerase) Homoeologous Genes and Promoter Sequences,” Gene, Vol. 366, No. 2, 2006, pp. 209-218. doi:10.1016/j.gene.2005.07.032
[32] A. P. Dhanapal, M. Ciaffi, E. Porceddu and E. d'Aloisio, “Protein Disulphide Isomerase Promoter Sequence Analysis of Triticum urartu, Aegilops speltoides and Aegilops tauschii,” Plant Genetic Resources, Vol. 9, No. 2, 2011, pp. 338-341. doi:10.1017/S147926211100013X
[33] M. A. Larkin, G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson and D. G. Higgins, “Clustal W and Clustal X Version 2.0,” Bioinformatics, Vol. 23, No. 21, 2007, pp. 2947-2948. doi:10.1093/bioinformatics/btm404
[34] N. Saitou and M. Nei, “The Neighbor-Joining Method: A New Method for Reconstructing Phylogenetic Trees,” Molecular Biology and Evolution, Vol. 4, No. 4, 1987, pp. 406-425.
[35] K. Tamura, J. Dudley, M. Nei and S. Kumar, “MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0,” Molecular Biology and Evolution, Vol. 24, No. 8, 2007, pp. 1596-1599. doi:10.1093/molbev/msm092
[36] F. Tajima, “Evolutionary Relationship of DNA Sequences in Finite Populations,” Genetics, Vol. 105, No. 2, 1983, pp. 437-460.
[37] M. Nei, “Molecular Evolutionary Genetics,” Columbia University Press, New York, 1987.
[38] G. A. Watterson, “On the Number of Segregating Sites in Genetic Models without Recombination,” Theoretical Population Biology, Vol. 7, No. 2, 1975, pp. 256-276. doi:10.1016/0040-5809(75)90020-9
[39] P. Librado and J. Rozas, “DnaSP v5: A Software for Comprehensive Analysis of DNA Polymorphism Data,” Bioinformatics, Vol. 25, No. 11, 2009, pp. 1451-1452. doi:10.1093/bioinformatics/btp187
[40] G. Kimber and M. Feldman, “Wild Wheat, an Introduction,” College of Agriculture University of Missouri Special Report, Vol. 353, Columbia, 1987, p. 146.
[41] M. van Slageren, “Wild Wheats: A Monograph of Aegilops L. and Amblyopyrum (Jaub. & Spach) Eig (Poaceae),” Wageningen Agriculture University Papers, Vol. 7, 1994, pp. 513.
[42] J. Dvorak, M. C. Luo, Z. L. Yang and H. B. Zhang, “The Structure of the Aegilops tauschii genepool and the Evolution of Hexaploid Wheat,” Theoritical and Applied Genetics, Vol. 97, No. 4, 1988b, pp. 657-670.
[43] P. Gitte, O. Seberg, M. Yde and K. Berthelsen, “Phylogenetic Relationships of Triticum and Aegilops and Evidence for the Origin of the A, B, and D Genomes of Common Wheat (Triticum aestivum),” Molecular Phylogenetics and Evolution, Vol. 39, No. 1, 2006, pp. 70-82. doi:10.1016/j.ympev.2006.01.023
[44] T. Simonite, “Ancient Genetic Tricks Shape up Wheat Turning Back the Evolutionary Clock Offers Better Crops for Dry Regions,” Nature, 2006.
[45] Y. X. Fu and W. H. Li, “Statistical Tests of Neutrality of Mutations,” Genetics, Vol. 133, No. 3, 1993, pp. 693-709.
[46] E. Tajima, “Statistical Test for Testing the Neutral Mutation Hypothesis by DNA Polymorphism,” Genetics, Vol. 123, No. 3, 1989, pp. 585-595.
[47] D. Charlesworth, C. Bartolome, M. H. Schierup and B. K. Mable, “Haplotype Structure of the Stigmatic Self-Incompatibility Gene in Natural Populations of Arabidopsis Iyrata,” Molecular Biology and Evolution, Vol. 20, No. 11, 2003, pp. 1741-1753. doi:10.1093/molbev/msg170
[48] N. C. Collins, T. Lahaye, C. Peterhansel, A. Freialdenhoven, M. Corbitt and P. Schulze-Lefert, “Sequence Haplotypes Revealed by Sequence-Tagged Site Fine Mapping of the Ror1 Gene in the Centromeric Region of Barley Chromosome 1H,” Plant Physiology, Vol. 125, No. 3, 2001, pp. 1236-1247. doi:10.1104/pp.125.3.1236
[49] M. Nordborg, J. O. Borevitz, J. Bergelson, C. C. Berry, J. Chory, J. Hagenblad, M. Kreitman, J. N. Maloof, T. Noyes, P. J. Oefner, E. A. Stahl and D. Weigel, “The Extent of Linkage Disequilibrium in Arabidopsis thaliana,” Nature Genetics, Vol. 30, No. 2, 2002, pp. 190-193. doi:10.1038/ng813
[50] A. Rafalski and M. Morgante, “Corn and Humans: Recombination and Linkage Disequilibrium in Two Genomes of Similar Size,” Trends in Genetics, Vol. 20, No. 2, 2004, pp. 103-111. doi:10.1016/j.tig.2003.12.002
[51] Y. L. Zhu, Q. J. Song, D. L. Hyten, C. P. Van Tassell, L. K. Matukumalli, D. R. Grimm, S. M. Hyatt, E. Fickus, N. D. Young and P. B. Cregan, “Single-Nucleotide Polymorphisms in Soybean,” Genetics, Vol. 163, No. 3, 2003, pp. 1123-1134.
[52] R. M. Clark, G. Schweikert, C. Toomajian, S. Ossowski, G. Zeller, P. Shinn, N. Warthmann, T. Hu, G. Fu, D. A. Hinds, H. Chen, K. A. Frazer, D. H. Huson, B. Sch?lkopf, M. Nordborg, G. R?tsch, J. R. Ecker and D. Weigel, “Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana,” Science, Vol. 317, No. 5836, 2007, pp. 338-342. doi:10.1126/science.1138632
[53] G. Zeller, R. M. Clark, K. Schneeberger, A. Bohlen, D. Weigel and G. R?tsch, “Detecting Polymorphic Regions in Arabidopsis thaliana with Resequencing Microarrays,” Genome Research, Vol. 18, No. 6, 2008, pp. 918-929. doi:10.1101/gr.070169.107
[54] D. A. Filatov and D. Charlesworth, “DNA Polymorphism, Haplotype Structure and Balancing Selection in the Leavenworthia PgiC Locus,” Genetics, Vol. 153, No. 3, 1999, pp. 1423-1434.

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