Genetically pyramiding protease-inhibitor genes for dual broad-spectrum resistance against insect and phytopathogens in transgenic tobacco

Plant Biotechnology Journal

Volumn 8, Issue 1, 2010, Pages 65-75

  Senthilkumar, Rajendran ^a   Cheng, Chiu Ping ^a   Yeh, Kai Wun ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Antibacterial activity; Antifungal activity; CeCPI (taro cystatin); Insect resistance; Sporamin; Synthetic wound inducible promoter (pMSPOA); Transgenic tobacco

Indexed keywords

CYSTATIN; PROTEINASE INHIBITOR; SPORAMIN PROTEIN, IPOMOEA BATATAS; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; COLOCASIA; ERWINIA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOTH; PLANT DISEASE; PROMOTER REGION; PYTHIUM; SWEET POTATO; TOBACCO; TRANSGENE; TRANSGENIC PLANT;

ANIMALS; COLOCASIA; CYSTATINS; ERWINIA; GENE EXPRESSION REGULATION, PLANT; IPOMOEA BATATAS; MOTHS; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEASE INHIBITORS; PYTHIUM; TOBACCO; TRANSGENES;

BACTERIA (MICROORGANISMS); COLOCASIA ESCULENTA; HELICOVERPA ARMIGERA; HEXAPODA; IPOMOEA BATATAS; NICOTIANA TABACUM; PECTOBACTERIUM CAROTOVORUM; PYTHIUM; PYTHIUM APHANIDERMATUM;

EID: 71949093356     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2009.00466.x     Document Type: Article

References (47)

1. Abdeen, A., Virgos, A., Olivella, E., Villanueva, J., Gabarra, R. Prat, S. (2005) Multiple insect resistance in transgenic tomato plants over expressing two families of plant proteinase inhibitors. Plant. Mol. Biol. 57, 184 202.
2. Abe, M., Abe, K., Kuroda, M. Arai, S. (1992) Corn kernel cysteine proteinase inhibitor as a novel cystatin superfamily member of plant origin molecular cloning and expression studies. Eur. J. Biochem. 209, 933 937.
3. Anand, A., Zhou, T., Trick, H.N., Gill, B.S., Bockus, W.W. Muthukrishnan, S. (2003) Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin- like protein, chitinase and glucanase against Fusarium graminearum. J. Exp. Bot. 54, 101 111.
4. Baena-González, E. Sheen, J. (2008) Convergent energy and stress signaling. Trends Plant Sci. 13, 474 482.
5. Bowles, D.J. (1990) Defense related proteins in higher plants. Annu. Rev. Biochem. 59, 873 907.
6. Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 254.
7. Cai, D., Thurau, T., Tian, Y., Lange, T., Yeh, K.W. Jung, C. (2003) Sporamin-mediated resistance to beet cyst nematodes (Heterodera schanchtii Schm.) is dependent on trypsin inhibitory activity in suar beet (Beta vulgaris L.) hairy roots. Plant Mol. Biol. 51, 839 849.
8. Chang, S., Puryean, J. Cairney, J. (1993) A simple and efficient method for isolating RNA from pine tree. Plant Mol. Biol. Rep. 11, 113 116.
9. Chen, H.J., Wang, S.J., Chen, C.C. Yeh., K.W. (2006) New gene construct strategy in T-DNA vector to enhance expression level of sweet potato sporamin and insect resistance in transgenic Brassica oleracea. Plant Sci. 171, 367 364.
10. Christou, P., Capell, T., Kohli, A., Gatehouse, J.A. Gatehouse, A.M.R. (2006) Recent development and future prospects in insect pest control in transgenic crops. Trends Plant Sci. 11, 302 308.
11. Doares, S.H., Syrovets, T., Weiler, E.W. Ryan, C.A. (1995) Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc. Natl Acad. Sci. U.S.A. 92, 4095 4098.
12. Estruch, J.J., Carozzi, N.B., Desai, N., Duck, N.B., Warren, G.W. Koziel, M.G. (1997) Transgenic plants: an emerging approach to pest control. Nat. Biotechnol. 15, 137 141.
13. Ferguson, A.J. Jeffers, S.N. (1999) Detecting multiple species of Phytophthora in container mixes from ornamental crop nurseries. Plant Dis. 83, 1129 1136.
14. Fernandes, K.V.S., Sabelli, P.A., Barratt, D.H.P., Richardson, M., Xavier- Filho, J. Shewry, P.R. (1993) The resistance of cowpea seeds to byuchid is not related to levels of cysteine proteinase inhibitors. Plant Mol. Biol. 23, 215 219.
15. Giudici, A.M., Regente, M.C. Canal, L. (2000) A potent antifungal protein from Helianthus annuus flowers is a trypsin inhibitor. Plant Physiol. Biochem. 38, 881 888.
16. Gutierrez-Campos, R., Torres-Acosta, J.A., Saucedo-Arias, L.J. Gomez-Lim, M.A. (1999) The use of cysteine proteinase inhibitors to engineer resistance against potyviruses in transgenic tobacco plants. Nat. Biotechnol. 17, 1223 1226.
17. Hardham, A.R. (2007) Cell biology of plant-oomycete interactions. Cell Microbiol. 9, 31 39.
18. Horsch, R.B., Fraley, R.T., Rogers, S.G., Sanders, P.R. Lloyd, A. (1985) A simple and general method for transferring genes into plants. Science, 227, 1229 1231.
19. Kazan, K. Manners, J.M. (2008) Jasmonate signaling: toward an integrated view. Plant Physiol. 146, 1459 1468.
20. Koiwa, H., Bressan, R.A. Hasegawa, P.M. (1997) Regulation of protease inhibitors and plant defense. Trends Plant Sci. 2, 379 384.
21. Koiwa, H., Shade, R.E., Salzman, K.Z., D'Urzo, M.P., Murdock, L.L. Bressan, R.A. (2000) A plant defensive cystatin (soyacystatin) targets cathepsin L-Like digestive cysteine proteinases (DvCALs) in the larval midgut of western corn rootworm (Diabrotica virgifera virgifera. FEBS Lett. 471, 67 70.
22. Liu, L., Kloepper, J.W. Tuzun, S. (1996) Induction of systemic resistance in cucumber against Fusarium wilt by plant growth promoting rhizobacteria. Phytopathology, 85, 695 698.
23. Maeshima, M., Sasaki, T. Asahi, T. (1985) Characterization of major proteins in sweet potato tuberous roots. Phytochemistry, 24, 1899 1902.
24. Martinez, M., Rubio-Somoza, I., Fuentes, R., Lara, P., Carbonero, P. Diaz, I. (2005) The barley cystatin gene (Icy) is regulated by DOF transcription factors in aleurone cells upon germination. J. Exp. Bot. 56, 547 556.
25. Masoud, S.A., Johnson, L.B., White, F.F. Reeck, G.R. (1993) Expression of proteinase inhibitor (ortza cystatin-I) in transgenic plants. Plant Mol. Biol. 21, 655 663.
26. Paulitz, T.C., Zhou, T. Rankin, L. (1992) Selection of rhizosphere bacteria for biological control of Pythium aphanidermatum on hydroponically grown cucumber. Biol. Control, 2, 226 237.
27. Pernas, M., Sánchez-Monge, R., Gómez, L. Salcedo, G. (1998) A chestnut seed cystatin differentially effective against cysteine proteinases from closely related pests. Plant. Mol. Biol. 38, 1235 1242.
28. Ryan, C.A. (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28, 425 449.
29. Sambrook, J. Russell, W.D. (2001) Molecular Cloning, A Laboratory Manual, 3rd edn. Cold Spring Harbor : Cold Spring Harbor Laboratory Press.
30. Schulze-Lefert, P. (2004) Knocking on the heaven's wall: pathogenesis of and resistance to biotrophic fungi at the cell wall. Curr. Opin. Plant Biol. 7, 377 383.
31. Sun, X.L., Wang, H.L., Sun, X.C., Chen, X.W., Peng, C.M., Pan, D.M., Jehle, J.A., Van der Werf, W., Vlak, J.M. Hu, Z.H. (2004) Biological activity and field efficacy of a genetically modified Helicoverpa armigera SNPV expressing an insect-selective toxin from a chimeric promoter. Biol. Control, 29, 124 137.
32. Terra, W.R. Ferreira, C. (1994) Insect digestive enzymes: properties, compartmentalization and function. Biochem. Physiol. 109b, 1 62.
33. Turk, V. Bode, W. (1991) The cystatins: protein inhibitors of cysteine proteinases. FEBS Lett. 285, 213 219.
34. Urwin, P.E., Atkinson, H.J., Waller, D.A. McPherson, M.J. (1995) Engineered oryzacystatin-I expressed in hairy roots confers resistance to Globodera pallida. Plant J. 8, 121 131.
35. Urwin, P.E., McPherson, M.J. Atkinson, H.J. (1998) Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs. Planta, 204, 472 479.
36. Walker, A.J., Urwin, P.E., Atkinson, H.J., Brain, P., Glen, D.M. Shewry, P.R. (1999) Transgenic Arabidopsis leaf tissue expressing a modified oryzacystatin shows resistance to the field slug Deroceras reticulatum (Müller). Transgenic Res. 8, 95 103.
37. Wang, S.J., Lan, Y.C., Chen, Y.M. Yeh, K.W. (2002) Woundresponsive regulation of the sweet potato sporamin gene promoter region. Plant Mol. Biol. 48, 223 231.
38. Wang, K., Senthil, K., Cheng, Y.S., Venkatagiri, S., Yang, A.H. Yeh, K.W. (2008) Characteriztion of mechanism and antifungl activity between group-1 and group-2 phytocystatin from taro (Colocasia esculenta). FEBS J. 275, 4980 4989.
39. Weigel, D. Glazebrook, J. (2002) Arabidopsis: A Laboratory Manual. Cold Spring Harbor, New York : Cold Spring Harbor Laboratory Press.
40. Wu, Y., Llewellyn, D., Matthews, A. Dennis, E.S. (1997) Adaptation of Helicoverpa armigera (Lepidoptera: Notuidae) to a proteinase inhibitor expressed in transgenic tobacco. Mol. Breed. 3, 371 380.
41. Xu, D., Xue, Q., McElroy, D., Mawal, Y., Hilder, V.A. Wu, R. (1996) Constitutive expression of a cowpea trypsin inhibitor gene, CpTi, in transgenic rice plants confers resistance to two major rice insect pests. Mol. Breed. 2, 167 173.
42. Yang, A.H. Yeh, K.W. (2005) Molecular cloning, recombinant gene expression, and antifungal activity of cystatin from taro (Colocasia esculenta cv. Kaosiung, 1). Planta, 221, 493 501.
43. Yao, P.E., Hwang, M.J., Chen, Y.M. Yeh, K.W. (2001) Site-directed mutagenesis evidence for a negatively charged trypsin inhibitory loop in sweet potato sporamin. FEBS Lett. 496, 134 138.
44. Yeh, K.-W., Lin, M.-I., Tuan, S.-J., Chen, Y.-M., Lin, C.-Y. Kao, S.-S. (1997a) Sweet potato (Ipomoea batatas)trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura. Plant Cell Rep. 16, 696 699.
45. Yeh, K.W., Chen, J.C., Lin, M.I., Chen, Y.M. Lin, C.Y. (1997b) Functional activity of sporamin from sweet potato (Ipomoeabatatas Lam.): a tuber storage protein with trypsin inhibitory activity. Plant Mol. Biol. 33, 565 570.
46. Zhao, Y., Botella, M.A., Subramanian, L., Niu, X., Nielsen, S.S. Bressan, R.A. (1996) Two wound-inducible soybean cysteine proteinase inhibitors have greater insect digestive proteinase inhibitory activities than a constitutive homolog. Plant Physiol. 111, 1299 1306.
47. Zhao, J.Z., Cao, J., Li, Y.X., Collins, H.L., Roush, R.T., Earle, E.D. Shelton, A.M. (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 21, 1493 1497.