Constitutive expression of a trypsin protease inhibitor confers multiple stress tolerance in transgenic tobacco

Plant and Cell Physiology

Volumn 50, Issue 3, 2009, Pages 541-553

  Srinivasan, Tantravahi ^a   Kumar, Koppolu Raja Rajesh ^a   Kirti, Pulugurtha Bharadwaja ^a  

^a UNIVERSITY OF HYDERABAD   (India)

Author keywords

Insect resistance; Osmotic stress tolerance; Protease inhibitor; Transgenic tobacco Wide pH range

Indexed keywords

HELICOVERPA ARMIGERA; HEXAPODA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; SPODOPTERA LITURA;

PLANT RNA; POTASSIUM; SODIUM; TRYPSIN INHIBITOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; HALOPHYTE; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PH; PHYSIOLOGICAL STRESS; PLANT GENE; TOBACCO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; BASE SEQUENCE; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POTASSIUM; RNA, PLANT; SALT-TOLERANT PLANTS; SEQUENCE ANALYSIS, DNA; SODIUM; STRESS, PHYSIOLOGICAL; TOBACCO; TRYPSIN INHIBITORS;

EID: 63049089591     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcp014     Document Type: Article

References (62)

1. Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts: poly phenoloxidase in Beta vulgaris. P lant Physiol. 24: 1-15.
2. Bacon, M.A., Thompson, D.S. and Davies, W.J. (1997) Can cell wall peroxidase activity explain the leaf growth response of Lolium temulentum L. during drought? J. Exp. Bot. 48: 2075-2085.
3. Bolter, C. and Jongsma, M.A. (1997) The adaptation of insects to plant protease inhibitors. J. Insect Physiol. 43: 885-895.
4. Broadway, R.M. (1995) Are insects resistant to plant protease inhibitors? J. Insect Physiol. 41: 107-116.
5. Brown, 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.
6. Callis, J. (1995) Regulation of protein degradation. P lant Cell 7: 845-857.
7. Capiati, D.A., PaIs, S.M. and Tellez-Inon, M.T. (2006) Wounding increases sodium chloride tolerance in tomato plants: evidence on the participation of calmodulin-like activities in cross tolerance signalling. J. Exp. Bot. 57: 2391-2400.
8. Charity, J.A., Anderson, M.A., Bittisnich, D.J., Whitecross, M. and Higgins, T.J.V. (1999) Transgenic tobacco and peas expressing a protease inhibitor from Nicotiana alata has increased insect resistance. Mol. Breed. 5: 357-365.
9. Chinnusamy, V., Schumaker, K. and Zhu, J.K. (2004) Molecular genetic perspectives on crosstalk and specifi city in abiotic stress signalling in plants. J. Exp. Bot. 55: 225-236.
10. Chinnusamy, V., Jagendorf, A. and Zhu, J.K. (2005) Understanding and improving sodium chloride tolerance in plants. Crop Sci. 45: 437-448.
11. Chougle, N.P., Hivrale, V.K., Chhabda, P.J., Giri, A.P. and Kachole, M.S. (2003) Differential inhibition of Helicoverpa armigera gut proteases by protease inhibitors of pigeon pea (Cajanus cajan) and its wild relatives. P hytochemistry 64: 681-687.
12. Conconi, A., Smerdon, M.J., Howe, G.A. and Ryan, C.A. (1996) The octadecanoid signalling pathway in plants mediates a response to ultraviolet radiation. N ature 383: 826-829.
13. Dombrowski, J.E. (2003) Sodium chloride stress activation of woundrelated genes in tomato plants. Plant Physiol. 132: 2098-2107.
14. Downing, W.L., Mauxion, F., Fauvarque, M.O., Reviron, M.P., de Vienne, D., Vartanian, N., et al. (1992) A Brassica napus transcript encoding a protein related to the Kunitz protease inhibitor family accumulates upon water stress in leaves, not in seeds. Plant J. 2: 685-693.
15. Felle, H.H. (2001) pH: signal and messenger in plant cells. P lant Biol. 3: 577-591.
16. Fugita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Shinozaki, K.Y., et al. (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. C urr. Opin. Plant Biol. 9: 436-442.
17. Gosti, F., Bertauche, N., Vartanian, N. and Giraudat, J. (1995) Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol. Gen. Genet. 246: 10-18.
18. Green, T.R. and Ryan, C.A. (1972) Wound-induced protease inhibitor in plant leaves: a possible defense mechanism against insects. Science 175: 776-777.
19. Heath, R.L. and Packer, L. (1968) Photoperoxidation in isolated chloroplasts. Kinetics and stochiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125: 189-198.
20. Hildermann, T., Ebneth, M., Cortth, H.P., Serrano, J.J.S., Willmitzer, L. and Prat, S. (1992) General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell 4: 1157-1170.
21. Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G. and Fraley, R.T. (1985) A simple and general method for transferring genes into plants. Science 227: 1229-1231.
22. Huang, Y., Xiao, B. and Xiong, L. (2007) Characterization of a stress responsive protease inhibitor gene with positive effect in improving drought resistance in rice. Planta 226: 73-85.
23. Iturbe-Ormaetxe, I., Escuredo, P.R., Arrese-Igor, C. and Becana, M. (1998) Oxidative damage in pea plants exposed to water defi cit or paraquat. P lant Physiol. 116: 173-181.
24. Johnson, R., Narvaez, J., An, G. and Ryan, C. (1989) Expression of protease inhibitors I and II in transgenic tobacco plants: effects on natural defense against manduca sexta larvae. Proc. Natl Acad. Sci. USA 86: 9871-9875.
25. Johnson, D.W., Smith, S.E. and Dobrenz, A.K. (1992) Genetic and phenotypic relationships in response to NaCl at different developmental stages in alfalfa. T heor. A ppl. Genet. 83: 833-838.
26. Jongsma, M.A. and Bolter, C.J. (1997) The adaptation of insects to plant protease inhibitors. J. Insect Physiol. 43: 885-895.
27. Kang, S.G., Choi, J.H. and Suh, S.G. (2002) A leaf-specifi c 27 kDa protein of potato Kunitz-type protease inhibitor is induced in response to abscisic acid, ethylene, methyl jasmonate, and water defi cit. Mol Cell 13: 144-147.
28. Klopfenstein, N.B., Allen, K.K., Avila, F.J., Heuchelin, S.A., Martinez, J., et al. (1997) Protease inhibitor II gene in transgenic poplar: chemical and biological assays. Biomass Bioenerg. 12: 299-311.
29. Kurkdjian, A. and Guern, J. (1989) Intracellular pH: measurement and importance in cell activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 271-303.
30. Lauchli, A., Epstein, E., (1990) Plant responses to saline and sodic conditions. In Agricultural Salinity Assessment and Management. Edited by Tanji, K.K. pp. 113-137. American Society of Civil Engineers, New York.
31. Lawrence, P.K. and Koundal, K.R. (2002) Plant protease inhibitors in control of phytophagous insects. Electronic J. Biotechnol. 5: 94-109.
32. Lee, M.C.S., Scanlon, M.J., Craik, D.J. and Anderson, M.A. (1999) A novel two-chain protease inhibitor generated by circularization of a multidomain precursor protein. Nat. Struct. Biol. 6: 526-530.
33. Lopez, F., Vansuyt, G., Derancourt, J., Fourcroy, P. and Casse-Delbart, F. (1994) Identifcation by 2D-page analysis of sodium chloride-stress induced proteins in radish (R aphanus sativus). C ell. Mol. Biol. 40: 85-90.
34. Mahajan, S. and Tuteja, N. (2005) Cold, salinity and drought stresses: an overview. A rch. Biochem. Biophys. 444: 139-158.
35. Mal, S., Gong, Q. and Bohnert, H.J. (2006) Dissecting salt stress pathways. J. Exp. Bot. 57: 1097-1107.
36. Malinowski, D.P. and Belesky, D.P. (2000) Adaptations of endophyteinfected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci. 40: 923-940.
37. Mazel, A., Leshem, Y., Tiwari, B.S. and Levine, A. (2004) Induction of sodium chloride and osmotic stress tolerance by overexpression of an intracellular vesicle traffi cking protein AtRab7 (AtRabG3e). Plant Physiol. 134: 118-128.
38. Miller, E.A., Lee, M.C.S., Atkinson, A.H.O. and Anderson, M. (2000) Identifi cation of a novel four-domain member of the protease inhibitor II family from the stigmas of Nicotiana alata. Plant Mol. Biol. 42: 329-333.
39. Mittler, R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7: 405-410.
40. Mukhopadhyay, A., Vij, S. and Tyagi, A.K. (2004) Overexpression of a zinc-fi nger protein gene from rice confers tolerance to cold, dehydration, and sodium chloride stress in transgenic tobacco. Proc. Natl Acad. Sci. USA 101: 6309-6314.
41. Murray, M.G. and Thompson, W.F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 19: 4321-4326.
42. Pearce, G., Johnson, S. and Ryan, C.A. (1993) Purifi cation and characterization from tobacco (Nicotiana tabacum) leaves of six small, wound-inducible, protease isoinhibitors of the potato inhibitor II family. Plant Physiol. 102: 639-644.
43. Pena-Cortes, H., Fisahn, J. and Willmitzer, L. (1995) Signals involved in wound-induced protease inhibitor II gene expression in tomato and potato plants. P roc. Natl Acad. Sci. USA 92: 4106-4113.
44. Pernas, M., Sanchez-Monge, R. and Salcedo, G. (2000) Biotic and abiotic stress can induce cystatin expression in chestnut. FEBS Lett. 467: 206-210.
45. Quander, H. and Fast, H. (1990) Infl uence of cytosolic pH changes on the organisation of the endoplasmic reticulum in epidermal cells of onion bulb scales: acidifi cation by loading with weak organic acids. Protoplasma 157: 216-224.
46. Richardson, M.J., (1991) Seed storage proteins: the enzyme inhibitors. In Methods in Plant Biochemistry. Edited by Richardson, M.J. pp. 259-305. Academic Press, New York.
47. Ryan, C.A. (1990) Protease inhibitors in plants: genes for improving defense against insects and pathogens. Annu. Rev. Phytopathol. 28: 25-49.
48. Sahi, C., Singh, A., Blumwald, E. and Grover, A. (2006) Beyond osmolytes and transporters: novel salt stress resistance genes from transcriptional profi ling data. Physiol. Plant. 127: 1-9.
49. Sajani, L.S. and Maruthi Mohan, P. (1997) Characterization of a cobaltresistant mutant of Neurospora crassa with transport block. BioMetals 10: 175-183.
50. Sambrook, J., Fritsch, E.F., Maniatis, T., (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Habor Laboratory Press, Cold Spring Harbor, NY.
51. Satoh, H., Uchida, A., Nakayama, K. and Okada, M. (2001) Watersoluble chlorophyll protein in Brassicaceae plants is a stress induced chlorophyll-binding protein. P lant Cell Physiol. 42: 906-911.
52. Schaller, A. and Ryan, C.A. (1995) Systemin: a polypeptide defense signal in plants. Bioessays 18: 27-33.
53. Shan, L., Li, C., Chen, F., Zhao, S. and Xia, G. (2008) A Bowman-Birk type protease inhibitor is involved in the tolerance to salt stress in wheat. Plant Cell Environ. 31: 1128-1137.
54. Sharma, H.C., Pampathy, G., Dhillon, M.K. and Smith, J.T.R. (2005) Detached leaf assay to screen for host plant resistance to Helicoverpa armigera. J. Econ. Entomol. 98: 568-576.
55. Sheoran, I.S. and Garg, O.P. (1978) Effect of salinity on the activities of RNase, DNase and protease during germination and early seedling growth of mung bean. Physiol. Plant. 44: 171-174.
56. Song, C.P., Guo, Y., Qiu, Q., Lambert, G., Galbraith, D.W., Jagendorf, A., et al. (2004) A probable Na + (K +)/H + exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 101: 10211-10216.
57. Telang, M., Srinivasan, A., Patankar, A., Harsulkar, A., Joshi, V., Damle, A., et al. (2003) Bitter gourd protease inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry 63: 643-652.
58. Timmusk, S. and Wagner, E.G.H. (1999) The plant-growth-promoting Rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol. Plant-Microbe Interact. 12: 951-959.
59. Vranova, E., Inze, D. and Breusegem, F.V. (2002) Signal transduction during oxidative stress. J. Exp. Bot. 53: 1227-1236.
60. Zavala, J.A., Patankar, A.G., Gase, K., Hui, D. and Baldwin, I.T. (2004) Manipulation of endogenous trypsin protease inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defences. P lant Physiol. 134: 1181-1190.
61. Zhou, S., Chen, X., Zhang, X. and Li, Y. (2008) Improved sodium chloride tolerance in tobacco plants by co-transformation of a betaine synthesis gene BADH and a vacuolar Na+/H+ antiporter gene SeNHX1. B iotechnol. Lett. 30: 369-376.
62. Zhu, J.K. (2001) Plant sodium chloride tolerance. T rends Plant Sci. 6: 1360-1385.