Protease inhibitors (PIs) are generally small proteins that have been identified in plants. The wip1 gene codes for wound-induced protein, which is similar to serine PIs of the Bowman-Birk family (BBIs). In this study, we analyzed 10 wip1 genes of Turkish maize varieties to understand the structure and characteristics of the wip1 genes and proteins in maize. We found that genetic variability of wip1 genes was higher (π: 0.0173) than reported in previous studies. Tajima’s D value was found to be positive (1.73), suggesting over-dominant selection in these loci. According to phylogenetic analysis of wip1 proteins, monocot and dicot BBIs were separated independently, and Turkish varieties were clustered with each other generally. The 3D structures of wip1 proteins indicated that several wip1 proteins had structural divergence in active loops, containing various numbers of cysteine residues ranging between 7 and 9. Particularly, Cys74 was identified in Kocbey and Gozdem varieties, whereas Cys98 was only in the Gozdem variety. Also, a critical serine residue (Ser98) was observed in two varieties — Antbey and Batem Efe. These results can contribute to understanding the role of wip1 genes and corresponding proteins in maize.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
National Center for Biotechnology Information
Turkish maize varieties
Barrett, A. J., Rawlings, N. D., and Brien, E. A. (2001) The MEROPS database as a protease information system, J. Struct. Biol., 14, 95–102.
Joanitti, G. A., Freitas, S. M., and Silva, L. P. (2006) Proteinaceous protease inhibitors: structural features and multiple functional faces, Curr. Enzyme Inhib., 2, 199–217.
Habib, H., and Fazili, K. M. (2007) Plant protease inhibitors: a defense strategy in plants, Biotechnol. Mol. Biol. Rev., 2, 68–85.
De Leo, F., Ceci, L. R., Jouanin, L., and Gallerani, R. (2001) Analysis of mustard trypsin inhibitor-2 gene expression in response to developmental or environmental induction, Planta, 212, 710–717.
Ryan, C. A. (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens, Annu. Rev. Phytopathol., 28, 425–449.
Koiwa, H., Bressan, R. A., and Hasegawa, P. M. (1997) Regulation of protease inhibitors and plant defense, Trends Plant Sci., 2, 379–384.
Rawlings, N. D., Tolle, D. P., and Barrett, A. J. (2004) Evolutionary families of peptidase inhibitors, J. Biochem., 378, 705–716.
Mello, M. O., Tanaka, A. S., and Silva-Filho, M. C. (2003) Molecular evolution of Bowman-Birk type proteinase inhibitors in flowering plants, Mol. Phylogenet. Evol., 27, 103–112.
Birk, Y., Gertler, A., and Khalef, S. (1963) A pure trypsin inhibitor from soya beans, Biochem. J., 87, 281–284.
Bowman, D. E. (1946) Differentiation of soybean antitryptic factors, Proc. Soc. Exp. Biol. Med., 63, 547–550.
Odani, S., and Ikenaka, T. (1976) The amino acid sequence of two soybean double headed proteinase inhibitors and evolutionary consideration on the legume proteinase inhibitors, J. Biochem., 80, 641–643.
Prakash, B., Selvaraj, S., Murthy, M. R. N., Sreerama, Y. N., Rao, D. R., and Gowda, L. R. (1996) Analysis of the amino acid sequences of plant Bowman-Birk inhibitors, J. Mol. Evol., 42, 560–569.
Tashiro, M., Hashino, K., Shiozaki, M., Ibuki, F., and Maki, Z. (1987) The complete amino acid sequence of rice bran trypsin inhibitor, J. Biochem., 102, 297–306.
Tanaka, A. S., Sampaio, M. U., Mentele, R., Auerswald, E. A., and Sampaio, C. A. M. (1996) Sequence of a new Bowman-Birk inhibitor from Torresea acreana seeds and comparison with Torresea cearensis trypsin inhibitor (TcTI2), J. Protein Chem., 15, 553–560.
Tiffin, P., and Gaut, B. S. (2001) Molecular evolution of the wound-induced serine protease inhibitor Wip1 in Zea and related genera, Mol. Biol. Evol., 18, 2092–2101.
Rohrmeier, T., and Lehle, L. (1993) WIP1, a woundinducible gene from maize with homology to Bowman-Birk proteinase inhibitors, Plant Mol. Biol., 22, 783–792.
Anonymous (2005) FAO, Faostat, www.fao.org.
Tasdan, K. (2005) Maize Market in Turkey: PhD thesis, Institute of Natural and Applied Sciences University of Cukurova, Adana, Turkey.
Ilarslan, R., Kaya, Z., Tolun, A. A., and Bretting, P. K. (2001) Genetic variability among Turkish pop, flint and dent corn (Zea mays L. spp. mays) races: enzyme polymorphism, Euphytica, 122, 171–179.
Okumus, A. (2007) Genetic variation and relationship between Turkish flint maize landraces by RAPD markers, Am. J. Agr. Biol. Sci., 2, 49–53.
Comertpay, G., Baloch, F. S., Kilian, B., Ulger, A. C., and Ozkan, H. (2012) Diversity assessment of Turkish maize landraces based on fluorescent labeled SSR markers, Plant Mol. Biol. Rep., 30, 261–274.
Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., and Madden, T. (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction, BMC Bioinformatics, 13, 134.
Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 22, 4673–4680.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 28, 2731–2739.
Nei, M. (1987) Molecular Evolutionary Genetics, Columbia University, New York.
Watterson, G. A. (1975) On the number of segregating sites in genetic models without recombination, Theor. Popul. Biol., 7, 188–193.
Tajima, F. (1983) Evolutionary relationship of DNA sequences in finite populations, Genetics, 105, 437–460.
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism, Genetics, 123, 585–595.
Fu, Y., and Li, W. (1993) Statistical tests of neutrality of mutations, Genetics, 133, 693–709.
Librado, P., and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 25, 1451–1452.
Gasteiger, E. (2005) Protein identification and analysis tools on the ExPASy server, in The Proteomics Protocols Handbook (Walker, J. M., ed.) Humana Press, pp. 571–607.
Yu, C. S., Lin, C. J., and Hwang, J. K. (2006) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions, Protein Sci., 13, 1402–1406.
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene ontology: tool for the unification of biology, Nat. Genet., 25, 25–29.
McGuffin, L. J., and Jones, D. T. (2003) Improvement of the GenTHREADER method for genomic fold recognition, Bioinformatics, 19, 874–881.
Buchan, D. W. A., Minneci, F., Nugent, T. C. O., Bryson, K., and Jones, D. T. (2013) Scalable web services for the PSIPRED protein analysis workbench, Nucleic Acids Res., 41, 340–348.
Guex, N., Peitsch, M. C., and Schwede, T. (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective, Electrophoresis, 30, 162–173.
Moeller, D. A., and Tiffin, P. (2008) Geographic variation in adaptation at the molecular level: a case study of plant immunity genes, Evolution, 62, 3069–3081.
Leng, E. R., Tavcar, A., and Trifunovic, V. (1962) Maize of Southeastern Europe and its potential value in breeding programs elsewhere, Euphytica, 11, 263–272.
Qi, R. F., Song, Z. W., and Chi, C. W. (2005) Structural features and molecular evolution of Bowman-Birk protease inhibitors and their potential application, Acta Biochim. Biophys. Sin., 37, 283–292.
Christeller, J. T. (2005) Evolutionary mechanisms acting on proteinase inhibitor variability, FEBS J., 272, 5710–5722.
Bode, W., and Huber, R. (1992) Natural protein proteinase inhibitors and their interaction with proteinases, Eur. J. Biochem., 204, 433–451.
Song, H. K., Kim, Y. S., Yang, J. K., Moon, J., Lee, J. Y., and Suh, S. W. (1999) Crystal structure of a 16 kDa doubleheaded Bowman-Birk trypsin inhibitor from barley seeds at 1.9 resolution, J. Mol. Biol., 293, 1133–1144.
Lin, G. D., Bode, W., Huber, R., Chi, C. W., and Engh, R. A. (1993) The 0.25-nm X-ray structure of the Bowman-Birk-type inhibitor from mung bean in ternary complex with porcine trypsin, Eur. J. Biochem., 212, 549–555.
Brauer, A. B., Domingo, G. J., Cooke, R. M., Matthews, S. J., and Leatherbarrow, R. J. A. (2002) conserved cis peptide bond is necessary for the activity of Bowman-Birk inhibitor protein, Biochemistry, 41, 10608–10615.
Conticello, S. G., Gilad, Y., Avidan, N., Ben-Asher, E., Levy, Z., and Fainzilber, M. (2001) Mechanisms for evolving hypervariability: the case of conopeptides, Mol. Biol. Evol., 18, 120–131.
Laskowski, M., Kato, I., Ardelt, W., Cook, J., Denton, A., Empie, M. W., Kohr, W. J., Park, S. J., Parks, K., Schatzley, B. L., Schoenberger, O. L., Tashiro, M., Vichot, G., Whatley, H. E., Wieczorek, A., and Wieczorek, M. (1987) Ovomucoid third domains from 100 avian species: isolation, sequences, and hypervariability of enzyme-inhibitor contact residues, Biochemistry, 26, 202–222.
Published in Russian in Biokhimiya, 2014, Vol. 79, No. 8, pp. 1042–1051.
About this article
Cite this article
Filiz, E., Tombuloglu, H., Koc, I. et al. Characterization of wound-induced serine protease inhibitor (wip1) genes and proteins in Turkish maize varieties. Biochemistry Moscow 79, 836–844 (2014). https://doi.org/10.1134/S0006297914080124
- protease inhibitors
- wound-induced protein
- Bowman-Birk family
- Turkish maize