Modulating the proteinase inhibitory profile of a plant cystatin by single mutations at positively selected amino acid sites

Plant Journal

Volumn 48, Issue 3, 2006, Pages 403-413

  Kiggundu, Andrew ^a,b   Goulet, Marie Claire ^c   Goulet, Charles ^c   Dubuc, Jean François ^c   Rivard, Daniel ^c   Benchabane, Meriem ^c   Pépin, Geneviève ^c   Vyver, Christell Van Der ^a   Kunert, Karl ^a   Michaud, Dominique ^c  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b Kawanda Agricultural Research Institute   (Uganda)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

Cysteine proteinase inhibitors; Plant cystatins; Plant insect interactions; Positive selection; Site directed mutagenesis

Indexed keywords

CYSTATINS; CYSTEINE PROTEINASE INHIBITORS; HERBIVOROUS; POACEAE;

AMINO ACIDS; ENZYME INHIBITION; ENZYMES; MAXIMUM LIKELIHOOD ESTIMATION; MUTAGENESIS;

PLANTS (BOTANY);

AMINO ACID; CYSTATIN; CYSTEINE PROTEINASE INHIBITOR; PRIMER DNA;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CODON; MUTATION; NUCLEOTIDE SEQUENCE; STATISTICAL MODEL;

AMINO ACIDS; BASE SEQUENCE; CODON; CYSTATINS; CYSTEINE PROTEINASE INHIBITORS; DNA PRIMERS; LIKELIHOOD FUNCTIONS; MODELS, MOLECULAR; MUTATION;

AMINO ACIDS; ENZYMATIC ACTIVITY; ENZYMES; PLANTS;

DICOTYLEDONEAE; GLYCINE (ANGIOSPERM); INSECTA; LILIOPSIDA; LYCOPERSICON ESCULENTUM; MAGNOLIOPHYTA; POACEAE; SOLANACEAE;

EID: 33749997790     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02878.x     Document Type: Article

References (77)

1. Abe, K., Emori, Y., Kondo, H., Suzuki, K. and Arai, S. (1987) Molecular cloning of a cysteine proteinase inhibitor of rice (oryzacystatin). Homology with animal cystatins and transient expression in the ripening process of rice seeds. J. Biol. Chem. 262, 16793-16797.
2. Arai, S. and Abe, K. (2000) Cystatin-based control of insects, with special reference to oryzacystatin. In Recombinant Protease Inhibitors in Plants (Michaud, D., ed.). Georgetown, TX: Landes Bioscience, pp. 27-42.
3. Arai, S., Matsumoto, I., Emori, Y. and Abe, K. (2002) Plant seed cystatins and their target enzymes of endogenous and exogenous origin. J. Agric. Food Chem. 50, 6612-6617.
4. 1-proteinase inhibitor family: role of the hypervariable reactive center loop. Mol. Biol. Evol. 19, 718-727.
5. Becerra, J.X. (2003) Synchronous coadaptation in an ancient case of herbivory. Proc. Natl Acad. Sci. USA, 100, 12804-12807.
6. Belenghi, B., Acconcia, F., Trovato, M., Perazzolli, M., Bocedi, A., Polticelli, F., Ascenzi, P. and Delledonne, M. (2003) AtCYS1, a cystatin from Arabidopsis thaliana, suppresses hypersensitive cell death. Eur. J. Biochem. 270, 2593-2604.
7. Bielawski, J.P. and Yang, Z. (2003) Maximum likelihood methods for detecting adaptive evolution after gene duplication. J. Struct. Funct. Genom. 3, 201-212.
8. Bielawski, J.P., Dunn, K.A., Sabehi, G. and Béjà, O. (2004) Darwinian adaptation of proteorhodopsin to different light intensities in the marine environment. Proc. Natl Acad. Sci. USA, 101, 14824-14829.
9. Bishop, J.G., Dean, A.M. and Mitchell-Olds, T. (2000) Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc. Natl Acad. Sci. USA, 97, 5322-5327.
10. Björk, I., Brieditis, I. and Abrahamson, M. (1994) Probing the functional role of the N-terminal region of cystatins by equilibrium and kinetic studies of the binding of Gly-11 variants of recombinant human cystatin C to target proteinases. Biochem. J. 305, 513-518.
11. Bode, W., Engh, R., Musil, D., Thiele, U., Huber, R., Karshikov, A., Brzin, J., Kos, J. and Turk, V. (1988) The 2.0 Å crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO J. 7, 2593-2599.
12. Bolter, C.J. (1993) Methyl jasmonate induces papain inhibitor(s) in tomato leaves. Plant Physiol. 103, 1347-1353.
13. Bolter, C.J. and Jongsma, M.A. (1995) Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase inhibitors induced in potato leaves by methyl jasmonate. J. Insect Physiol. 41, 1071-1078.
14. Botella, M.A., Xu, Y., Prabha, T.N., Zhao, Y., Narasimhan, M.L., Wilson, K.A., Nielsen, S.S., Bressan, R.A. and Hasegawa, P.M. (1996) Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiol. 112, 1201-1210.
15. Bouchard, É., Cloutier, C. and Michaud, D. (2003) Oryzacystatin I expressed in transgenic potato induces digestive compensation in an insect natural predator via its herbivorous prey feeding on the plant. Mol. Ecol. 12, 2439-2446.
16. Bown, D.P., Wilkinson, H.S. and Gatehouse, J.A. (1997) Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem. Mol. Biol. 27, 625-638.
17. Ceci, L.R., Volpicella, M., Rahbé, Y., Gallerani, R., Beekwilder, J. and Jongsma, M.A. (2003) Selection by phage display of a variant mustard trypsin inhibitor toxic against aphids. Plant J. 33, 557-566.
18. Cloutier, C., Fournier, M., Jean, C., Yelle, S. and Michaud, D. (1999) Growth compensation and faster development of Colorado potato beetle (Coleoptera: Chrysomelidae) feeding on potato foliage expressing oryzacystatin I. Arch. Insect Biochem. Physiol. 40, 69-79.
19. Cloutier, C., Jean, C., Fournier, M., Yelle, S. and Michaud, D. (2000) Adult Colorado potato beetles, Leptinotarsa decemlineata, compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch. Insect Biochem. Physiol. 44, 69-81.
20. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucl. Acids Res. 16, 10881-10890.
21. Creighton, T.E. and Darby, N.J. (1989) Functional evolutionary divergence of proteolytic enzymes and their inhibitors. Trends Biochem. Sci. 14, 319-324.
22. Felsenstein, J. (1997) An alternative least-squares approach to inferring phylogenies from pairwise distances. Syst. Biol. 46, 101-111.
23. Garcia-Carreno, F.L. (1996) Proteinase inhibitors. Trends Food Sci. Technol. 7, 197-204.
24. Girard, C., Bonadé-Bottino, M., Pham-Delegue, M.-H. and Jouanin, L. (1998a) Two strains of cabbage seed weevil (Coleoptera: Curculionidae) exhibit differential susceptibility to transgenic oilseed rape expressing oryzacystatin-I. J. Insect Physiol. 44, 569-577.
25. Girard, C., Le Métayer, M., Bonadé-Bottino, M., Pham-Delègue, M.-H. and Jouanin, L. (1998b) High level of resistance to proteinase inhibitors conferred by proteolytic cleavage in beetle larvae. Insect Biochem. Mol. Biol. 28, 229-237.
26. Gruden, K., Kuipers, A.G.J., Guncar, G., Slapar, N., Strukelj, B. and Jongsma, M.A. (2004) Molecular basis of Colorado potato beetle adaptation to potato plant defence at the level of digestive cysteine proteinases. Insect Biochem. Mol. Biol. 34, 365-375.
27. Guttierrez-Campos, R., Torres-Acosta, J.A., Saucedo-Arias, L.J. and Gomez-Lin, M.A. (1999) The use of cysteine proteinase inhibitors to engineer resistance against potyviruses in transgenic tobacco plants. Nature Biotechnol. 17, 1223-1226.
28. Henderson, P.J.F. (1972) A linear equation that describes the steady-state kinetics of enzymes and subcellular particles interacting with tightly bound inhibitors. Biochem. J. 127, 321-333.
29. Henskens, Y.M.C., Veerman, E.C.I. and Nieuw Amerongen, A.V. (1996) Cystatins in health and disease. Biol. Chem. Hoppe-Seyler 377, 71-86.
30. Ivarsson, Y., Mackey, A.J., Edalat, M., Pearson, W.R. and Mannervik, B. (2003) Identification of residues in glutathione transferase capable of driving functional diversification in evolution. A novel approach to protein redesign. J. Biol. Chem. 278, 8733-8738.
31. Jacinto, T., Fernandes, K.V.S., Machado, O.L.T. and Siqueira-Junior, C.L. (1998) Leaves of transgenic tomato plants overexpressing prosystemin accumulate high levels of cystatin. Plant Sci. 138, 35-42.
32. Kimura, M. (1983) The Neutral Theory of Molecular Evolution. Cambridge, UK: Cambridge University Press.
33. Koiwa, H., Paino D'Urzo, M., Assfalg-Machleidt, I., Zhu-Salzman, K., Shade, R.E., An, H., Murdock, L.L., Machleidt, W., Bressan, R.A. and Hasegawa, P.M. (2001) Phage display selection of hairpin loop soyacystatin variants that mediate high affinity inhibition of a cysteine proteinase. Plant J. 27, 383-391.
34. Kondo, H., Abe, K., Nishimura, I., Watanabe, H., Emori, Y. and Arai, S. (1990) Two distinct cystatin species in rice seeds with different specificities against cysteine proteinases. Molecular cloning, expression, and biochemical studies on oryzacystatin-II. J. Biol. Chem. 265, 15832-15837.
35. Laboissière, M.C.A., Young, M.M., Pinho, R.G., Todd, S., Fletterick, R.J., Kuntz, I. and Craik, C.S. (2002) Computer-assisted mutagenesis of ecotin to engineer its secondary binding site for urokinase inhibition. J. Biol. Chem. 277, 26623-26631.
36. Lilley, C.J., Urwin, P.E., Johnston, K.A. and Atkinson, H.J. (2004) Preferential expression patterns of a plant cystatin at nematode feeding sites confers resistance to Meloidogyne and Globodera spp. Plant Biotechnol. J. 2, 3-12.
37. Lopes, A.R., Juliano, M.A., Juliano, L. and Terra, W.R. (2004) Coevolution of insect trypsins and inhibitors. Arch. Insect Biochem. Physiol. 55, 140-152.
38. Lynch, M. and Conery, J.S. (2000) The evolutionary fate and consequences of duplicate genes. Science, 290, 1151-1155.
39. Lynn, D.J., Lloyd, A.T., Fares, M.A. and O'Farrelly, C. (2004) Evidence of positively selected sites in mammalian α-defensins. Mol. Biol. Evol. 21, 819-827.
40. Machleidt, W., Thiele, U., Laber, B., Assfalg-Machleidt, I., Esterl, A., Wiegand, G., Kos, J., Turk, V. and Bode, W. (1989) Mechanism of inhibition of papapin by chicken egg white cystatin. Inhibition constants of N-terminally truncated forms and cyanogen bromide fragments of the inhibitor. FEBS Lett. 243, 234-238.
41. Margis, R., Reis, E.M. and Villeret, V. (1998) Structural and phylogenetic relationships among plant and animal cystatins. Arch. Biochem. Biophys. 359, 24-30.
42. Martinez, M., Abraham, Z., Gambardella, M., Echaide, M., Carbonero, P. and Diaz, I. (2005) The strawberry gene Cyf1 encodes a phytocystatin with antifungal properties. J. Exp. Bot. 56, 1821-1829.
43. Mason, R.W., Sol-Church, K. and Abrahamson, M. (1998) Amino acid substitutions in the N-terminal segment of cystatin C create selective protein inhibitors of lysosomal cysteine proteinases. Biochem. J. 330, 833-838.
44. Mauricio, R. and Rausher, M.D. (1997) Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution, 53, 1435-1444.
45. Mazumdar-Leighton, S. and Broadway, R.M. (2001a) Identification of six chymotrypsin cDNAs from larval midguts of Helicoverpa zea and Agrotis ipsilon feeding on the soybean (Kunitz) trypsin inhibitor. Insect Biochem. Mol. Biol. 31, 633-644.
46. Mazumdar-Leighton, S. and Broadway, R.M. (2001b) Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochem. Mol. Biol. 31, 645-657.
47. Michaud, D. (1997) Avoiding protease-mediated resistance in herbivorous pests. Trends Biotechnol. 15, 4-6.
48. Michaud, D., Nguyen-Quoc, B. and Yelle, S. (1994) Production of oryzacystatins I and II in Escherichia coli using the glutathione S-transferase gene fusion system. Biotechnol. Progr. 10, 155-159.
49. Michaud, D., Bernier-Vadnais, N., Overney, S. and Yelle, S. (1995a) Constitutive expression of digestive cysteine proteinase forms during development of the Colorado potato beetle, Leptinotarsa decemlineata Say (Coloeptera: Chrysomelidae). Insect Biochem. Mol. Biol. 25, 1041-1048.
50. Michaud, D., Cantin, L. and Vrain, T.C. (1995b) Carboxy-terminal truncation of oryzacystatin II by oryzacystatin-insensitive insect digestive proteinases. Arch. Biochem. Biophys. 322, 469-474.
51. Michaud, D., Cantin, L., Bonadé-Bottino, M., Jouanin, L. and Vrain, T.C. (1996) Identification of stable plant cystatin/nematode proteinase complexes using mildly-denaturing gelatin polyacrylamide gel electrophoresis. Electrophoresis, 17, 1373-1379.
52. Moon, J., Salzman, R.A., Ahn, J.-E., Koiwa, H. and Zhu-Salzman, K. (2004) Transcriptional regulation in cowpea bruchid guts during adaptation to a plant defence protease inhibitor. Insect Mol. Biol. 13, 283-291.
53. Murdock, L.L., Brookhart, G., Dunn, P.E., Foard, D.E., Kelly, S., Kitch, L., Shade, R.E., Shukle, R.H. and Wolfson, J.L. (1987) Cysteine digestive proteinases in Coleoptera. Comp. Biochem. Physiol. B, 87, 783-787.
54. Nagata, K., Kudo, N., Abe, K., Arai, S. and Tanokura, M. (2000) Three-dimensional solution structure of oryzacystatin-I, a cysteine proteinase inhibitor of the rice, Oryza sativa L. japonica. Biochemistry, 39, 14753-14760.
55. Ogawa, M., Nakamura, S., Scaman, C.H., Jing, H., Kitts, D.D., Dou, J. and Nakai, S. (2002) Enhancement of proteinase inhibitory activity of recombinant human cystatin C using random-centroid optimization. Biochim. Biophys. Acta, 1599, 115-124.
56. Pavlova, A. and Björk, I. (2003) Grafting of features of cystatins C or B into the N-terminal region or second binding loop of cystatin A (stefin A) substantially enhances inhibition of cysteine proteinases. Biochemistry, 42, 11326-11333.
57. Qasim, M.A., Ganz, P.J., Saunders, C.W., Bateman, K.S., James, M.N.G. and Laskowski, M. (1997) Interscaffolding activity. Association of p1 variants of eglin c and of turkey ovomucoid third domain with serine proteinase. Biochemistry, 36, 1598-1607.
58. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
59. Salvesen, G. and Nagase, H. (1989) Inhibition of proteolytic enzymes. In Proteolytic Enzymes. A Practical Approach (Bond, J.S. and Beynon, R., eds). New York: IRL Press, pp. 83-104.
60. Sawyer, S.L., Wu, L.I., Emerman, M. and Malik, H.S. (2005) Positive selection of primate TRIM5α identifies a critical species-specific retroviral restriction domain. Proc. Natl Acad. Sci. USA, 102, 2832-2837.
61. Shonle, I. and Bergelson, J. (2000) Evolutionary ecology of the tropane alkaloids of Datura stramonium L. (Solanaceae). Evolution, 54, 778-788.
62. Soares-Costa, A., Beltramini, L.M., Thiemann, O.H. and Henrique-Silva, F. (2002) A sugarcane cystatin: recombinant expression, purification, and antifungal activity. Biochem. Biophys. Res. Commun. 296, 1194-1199.
63. Stoop, A.A. and Craik, C.S. (2003) Engineering of a macromolecular scaffold to develop specific protease inhibitors. Nature Biotechnol. 21, 1063-1068.
64. Stubbs, M.T., Laber, B., Bode, W., Huber, R., Jerala, R., Lenarcic, B. and Turk, V. (1990) The refined 2.4 Å X-ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction. EMBO J. 9, 1939-1947.
65. Terra, W.R. and Ferreira, C. (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. B, 109, 1-62.
66. Tiffin, P. and Gaut, B.S. (2001) Molecular evolution of the woundinduced serine protease inhibitor wip1 in Zea and related genera. Mol. Biol. Evol. 18, 2092-2101.
67. Turk, B., Turk, V. and Turk, D. (1997) Structural and functional aspects of papain-like cysteine proteinases and their protein inhibitors. Biol. Chem. 378, 141-150.
68. Urwin, P.E., Atkinson, H.J., Waller, D.A. and McPherson, M.J. (1995) Engineered oryzacystatin-I expressed in transgenic hairy roots confers resistance to Globodera pallida. Plant J. 8, 121-131.
69. Van der Vyver, C., Schneidereit, J., Driscoll, S., Turner, J., Kunert, K. and Foyer, C.H. (2003) Oryzacystatin I expression in transformed tobacco produces a conditional growth phenotype and enhances chilling tolerance. Plant Biotechnol. J. 1, 101-112.
70. Waldron, C., Wegrich, L.M., Merlo, P.A.O. and Walsh, T.A. (1993) Characterization of a genomic sequence coding for potato multicystatin, an eight-domain cysteine proteinase inhibitor. Plant Mol. Biol. 23, 801-812.
71. Wang, Y., Geer, L.Y., Chappey, C., Kans, J.A. and Bryant, S.H. (2000) Cn3D: sequence and structure views for Entrez. Trends Biochem. Sci. 25, 300-302.
72. Yang, Z. (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556.
73. Yang, Z. (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15, 568-573.
74. Yang, Z. (2005) The power of phylogenetic comparison in revealing protein function. Proc. Natl Acad. Sci. USA, 102, 3179-3180.
75. Yang, Z. and Bielawski, J.P. (2000) Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496-503.
76. Yang, Z., Nielsen, R., Goldman, N. and Pedersen, A.-M.K. (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics, 155, 431-449.
77. Zhu-Salzman, K., Koiwa, H., Salzman, R.A., Shade, R.E. and Ahn, J.-E. (2003) Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol. Biol. 12, 135-145.