Skip to main content
Log in

Inhibitory properties and binding loop polymorphism in Bowman-Birk inhibitors from Phaseolus species

  • Research Article
  • Published:
Genetic Resources and Crop Evolution Aims and scope Submit manuscript

Abstract

The primary structure of the double-headed Bowman-Birk inhibitor (BBI) family and the antitryptic activity were investigated in cultivated and wild Phaseolus species. Two BBI types were identified; the first one inhibits trypsin and chymotrypsin (tc-BBI), the second one elastase and trypsin (et-BBI). Only tc-BBI was found in P. lunatus and P. parvulus, while none of BBI types, identified in this study, was found in P. leptostachyus. The deduced amino acid sequences revealed some polymorphisms within both tc-BBI and et-BBI binding loops that could affect the inhibitory activity. The trypsin inhibitor content showed a high variation with the lowest value recorded in P. lepthostachyus and the highest one observed in P. oligospermus. Southern blot analysis confirmed the absence of both BBI types in P. leptostachyus and suggests that in P. coccineus, P. dumosus and P. costaricensis, the two genes were clustered in a narrow genomic region of 1.3 kbp.

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

Similar content being viewed by others

References

  • Armstrong WB, Wan XS, Kennedy AR, Taylor TH (2003) Development of the Bowman-Birk inhibitor for oral cancer chemoprevention and analysis of Neu immunohistochemical staining intensity with Bowman-Birk inhibitor concentrate treatment. Laryngoscope 113:1687–1702

    Article  CAS  PubMed  Google Scholar 

  • Birk Y, Gertler A, Khalef S (1963) Heat inactivation of trypsin inhibitor from soybeans. Biochem J 87:281–284

    CAS  PubMed  Google Scholar 

  • Brauer ABE, Kelly G, Matthews SJ, Leatherbarrow RJ (2002) The H1 NMR solution structure of the antitryptic core peptide of Bowman-Birk inhibitor proteins: a minimal ‘Canonical loop’. J Biomol Struct Dyn 20:59–70

    CAS  PubMed  Google Scholar 

  • Campos JE, Whitaker JR, Yip TT, Hutchens TW, Blanco-Labra A (2004) Unusual structural characteristics and complete amino acid sequence of a protease inhibitor from Phaseolus acutifolius seeds. Plant Physiol Biochem 42:209–214. doi:10.1016/j.plaphy.2003.12.002

    Article  CAS  PubMed  Google Scholar 

  • Carlini CR, Grossi-de-Sa MF (2002) Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 40:1515–1539

    Article  CAS  PubMed  Google Scholar 

  • De Azevedo Pereira R, Valencia-Jiménez A, Picanço Magalhães C et al (2007) Effect of a Bowman-Birk proteinase inhibitor from Phaseolus coccineus on Hypothenemus hampei gut proteinases in vitro. J Agric Food Chem 55:10714–19719. doi:10.1021/jf072155x

    Article  PubMed  Google Scholar 

  • Debouck DG (2000) Biodiversity, ecology and genetic resources of Phaseolus beans—seven answered and unanswered questions. In: Prooc 7th MAFF Int Workshop Genet Resour Part 1 Wild Legumes AFFRC et NIAR, Japan

  • Delgado-Salinas A, Turley T, Richman A, Lavin M (1999) Phylogenetic analysis of the cultivated and wild species of Phaseolus (Fabaceae). Syst Bot 24:438–460

    Article  Google Scholar 

  • Delgado-Salinas A, Bibler R, Lavin M (2006) Phylogeny of the genus Phaseolus (Leguminosae): a recent diversification in an ancient landscape. Syst Bot 31:779–791

    Article  Google Scholar 

  • Della Gatta C, Piergiovanni AR, Perrino P (1988) An improved method for the determination of trypsin inhibitor level in legumes. Lebensm Wiss Technol 21:315–318

    CAS  Google Scholar 

  • Domoney C, Welham T, Sidebottom C, Firmin JL (1995) Multiple isoforms of Pisum trypsin inhibitors result from modification of two primary gene products. FEBS Letters 360:15–20

    Article  CAS  PubMed  Google Scholar 

  • Freytag GF, Debouck DG (2002) Taxonomy, distribution, and ecology of the genus Phaseolus (Leguminosae-Papilionoideae) in North America, Mexico and Central America. SIDA, Botanical Miscellany 23 (1–300)

  • Galasso I, Piergiovanni AR, Lioi L, Campion B, Bollini R, Sparvoli F (2009) Bowman-Birk inhibitors in common bean. Mol Breeding 23:617–624

    Article  CAS  Google Scholar 

  • Gariani T, McBride JD, Leatherbarrow RJ (1999) The role of the P2′ position of Bowman-Birk proteinase inhibitor in the inhibition of trypsin. Studies on P2′ variation in cyclic peptides encompassing the reactive site loop. Biochem Biophys Acta 1431:232–237

    CAS  PubMed  Google Scholar 

  • Jacobsen BK, Knutsen SF, Fraser GE (1998) Does high soy milk intake reduce prostate cancer incidence? The Adventist Health Study (United States). Cancer Causes Control 9:553–557

    Article  CAS  PubMed  Google Scholar 

  • Kennedy AR, Billings PC, Wan XS, Wan PM (2002) Effects of Bowman-Birk inhibitor on rat colon carcinogesesis. Nutr Cancer 43:174–186

    Article  CAS  PubMed  Google Scholar 

  • Laskowski M, Kato I (1980) Protein inhibitors of proteinases. Annu Rev Biochem 49:593–626

    Article  CAS  PubMed  Google Scholar 

  • Lioi L, Galasso I, Lanave C, Daminati MG, Bollini R, Sparvoli F (2007) Evolutionary analysis of the APA genes in the Phaseolus genus: wild beans as source of lectin-related resistance factors? Theor App Genet 115:959–970. doi:10.1007/s00122-007-0622-1

    Article  CAS  Google Scholar 

  • McBride JD, Freeman HNM, Leatherbarrow RJ (1999) Selection of human elastase inhibitors from a conformationally constrained combinatorial peptide library. Eur J Biochem 266:403–412

    Article  CAS  PubMed  Google Scholar 

  • Mello MO, Tanaka AS, Silva-Filho MC (2003) Molecular evolution of Bowman-Birk type proteinase inhibitors in flowering plants. Mol Phylog Evol 27:103–112. doi:10.1016/S1055-7903(02)00373-1

    Article  CAS  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 2:129–134

    Article  Google Scholar 

  • Molsov VV, Valueva TA (2005) Proteinase inhibitors and their function in plants: a review. Appl Biochem Microbiol 41:227–246

    Article  Google Scholar 

  • Morrison SC, Savage GP, Morton JD, Russell AC (2007) Identification and stability of trypsin inhibitor isoforms in pea (Pisum sativum L.) cultivars grown in New Zealand. Food Chem 100:1–7. doi:10.1016/j.foodchem.2005.07.062

    Article  CAS  Google Scholar 

  • Odani S, Ikenaka T (1973) Studies on soybean trypsin inhibitors. 8. Disulfide bridges in soybean Bowman-Birk inhibitors. J Biochem (Tokio) 74:697–715

    CAS  Google Scholar 

  • Odani S, Ono T (1980) Chemical substitution of the reactive site leucine residue in soybean Bowman-Birk proteinase inhibitor with others amino acids. J Biochem 88:1555–1558

    CAS  PubMed  Google Scholar 

  • Piergiovanni AR, Galasso I (2004) Polymorphism of trypsin and chymotrypsin binding loops in Bowman-Birk inhibitors from common bean (Phaseolus vulgaris L.). Plant Sci 166:1525–1531. doi:10.1002/jsfa.1404

    Article  CAS  Google Scholar 

  • Piergiovanni AR, Pignone D (2003) Effect of year-to-year variation and genotype on trypsin inhibitor level in common bean (Phaseolus vulgaris L.) seeds. J Sci Food Agric 83:473–476. doi:10.1016/J.plantsci.2004.02.005

    Article  CAS  Google Scholar 

  • Prakash B, Selvaraj S, Murthy MR, Sreerama YN, Rao DR, Gowda LR (1996) Analysis of amino acid sequences of plant Bowman-Birk protease inhibitors. J Mol Evol 42:560–569

    Article  CAS  PubMed  Google Scholar 

  • Rui-Feng Q, Zhan-Wu S, Cheng-Wu C (2005) Structural features and molecular evolution of Bowman-Birk protease inhibitors and their potential application. Acta Biochim Biophys Sinica 37:283–292. doi:10.1111/j.1745-7270.2005.00048.x

    Article  Google Scholar 

  • Ryan CA (1990) Protease inhibitors in plants: genes for improving defences against insects and pathogens. Annu Rev Phytopathol 28:425–449

    Article  CAS  Google Scholar 

  • Scarafoni A, Consonni A, Galbusera V, Negri A, Tedeschi G, Rasmussen P, Magni C, Duranti M (2008) Identification and characterization of a Bowman-Birk inhibitor active towards trypsin but not chymotrypsin in Lupinus albus seeds. Phytochem 69:1820–1825. doi:10.1016/j.phytochem.2008.03.023

    Article  CAS  Google Scholar 

  • Schechter J, Berger A (1967) On the size of the active site proteases I Papain. Biochem Biophys Res Commun 27:157–162

    Article  CAS  PubMed  Google Scholar 

  • Ware JH, Wan XS, Newberne P, Kennedy AR (1999) Bowman-Birk inhibitor concentrate reduces colon inflammation in mice with dextran sulfate sodium-induced ulcerative colitis. Dig Dis Sci 44:986–990

    Article  CAS  PubMed  Google Scholar 

  • Wilson KA, Laskowski MS (1975) The partial amino acid sequence of trypsin inhibitor II from garden bean, Phaseolus vulgaris, with location of the trypsin and elastase-reactive sites. J Biol Chem 250:4261–4267

    CAS  PubMed  Google Scholar 

  • Wu C, Whitaker JR (1990) Purification and partial characterisation of four trypsin/chymotrypsin inhibitors from red kidney beans (Phaseolus vulgaris var. Linden). J Agric Food Chem 38:1523–1529

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Research partially supported by Ministry of Agriculture Food and Forestry Policies with funds released by C.I.P.E (Resolution 17/2003).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucia Lioi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 32 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lioi, L., Galasso, I., Daminati, M.G. et al. Inhibitory properties and binding loop polymorphism in Bowman-Birk inhibitors from Phaseolus species. Genet Resour Crop Evol 57, 533–542 (2010). https://doi.org/10.1007/s10722-009-9491-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10722-009-9491-6

Keywords

Navigation