A translationally controlled tumor protein negatively regulates the hypersensitive response in nicotiana benthamiana

Plant and Cell Physiology

Volumn 54, Issue 8, 2013, Pages 1403-1414

  Gupta, Meenu ^a   Yoshioka, Hirofumi ^b   Ohnishi, Kouhei ^a   Mizumoto, Hiroyuki ^a   Hikichi, Yasufumi ^a   Kiba, Akinori ^a  

^a KOCHI UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

Hypersensitive response; Nicotiana benthamiana; Translationally controlled tumor protein; Virus induced gene silencing

Indexed keywords

AGROBACTERIUM; NICOTIANA; NICOTIANA BENTHAMIANA; PSEUDOMONAS; PSEUDOMONAS CICHORII; PSEUDOMONAS SYRINGAE PV. SYRINGAE; RALSTONIA SOLANACEARUM;

PLANT DNA; REACTIVE OXYGEN METABOLITE; TRANSLATIONALLY CONTROLLED TUMOR PROTEIN; VEGETABLE PROTEIN;

ALLERGIC REACTION; AMINO ACID SEQUENCE; ARTICLE; CELL DEATH; CHEMISTRY; DNA SEQUENCE; GENE SILENCING; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NICOTIANA BENTHAMIANA; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PROTEIN TERTIARY STRUCTURE; PSEUDOMONAS; RALSTONIA SOLANACEARUM; TOBACCO; VIRUS-INDUCED GENE SILENCING;

HYPERSENSITIVE RESPONSE; NICOTIANA BENTHAMIANA; TRANSLATIONALLY CONTROLLED TUMOR PROTEIN; VIRUS-INDUCED GENE SILENCING;

AMINO ACID SEQUENCE; BASE SEQUENCE; CELL DEATH; DNA, PLANT; GENE SILENCING; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS; RALSTONIA SOLANACEARUM; REACTIVE OXYGEN SPECIES; SEQUENCE ANALYSIS, DNA; TOBACCO;

EID: 84881437199     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct090     Document Type: Article

References (68)

1. Abramovitch, R.B., Kim, Y.J., Chen, S., Dickman, M.B. and Martin, G.B. (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22: 60-69. (Pubitemid 36091269)
2. Altschul, S.F., Gish, W., Miller, W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Anand, A., Uppalapati, S.R., Ryu, C.-M., Allen, S.N., Kang, L., Tang, Y. et al. (2008) Salicylic acid and systemic acquired resistance play a role in attenuating crown gall disease caused by Agrobacterium tumefaciens. Plant Physiol. 146: 703-715. (Pubitemid 351230798)
4. Asai, S., Mase, K. and Yoshioka, H. (2010) A key enzyme for flavin synthesis is required for nitric oxide and reactive oxygen species production in disease resistance. Plant J. 62: 911-924.
5. Asai, S., Ohta, K. and Yoshioka, H. (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20: 1390-1406. (Pubitemid 352844190)
6. Asai, S. and Yoshioka, H. (2009) Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nicotiana benthamiana. Mol. Plant-Microbe Interact. 22: 619-629.
7. Baker, C.G. and Orlandi, E.W. (1995) Active oxygen in plant pathogen-esis. Annu. Rev. Phytopathol. 33: 299-321.
8. Baulcombe, D.C., Chapman, S. and Cruz, S.S. (1995) Jellyfish green fluorescent protein as a reporter for virus infections. Plant J. 7: 1045-1053.
9. Beers, E.P. and McDowell, J.M. (2001) Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Curr. Opin. Plant Biol. 4: 561-567. (Pubitemid 33001808)
10. Benoit, J.B. and Dangl, J.L. (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4: 671-683. (Pubitemid 127680703)
11. Berkowitz, O., Jost, R., Pollmann, S. and Maslea, J. (2008) Characterization of TCTP, the translationally controlled tumor protein, from Arabidopsis thaliana. Plant Cell 20: 3430-3447.
12. Boller, T. and Felix, G. (2009) A renaissance of elicitors: perception of microbe-associated molecular pattern and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60: 379-406.
13. Bommer, U.A. and Thiele, B.J. (2004) The translationally controlled tumour protein (TCTP). Int. J. Biochem. Cell Biol. 36: 379-385.
14. Bradly, D., Kjellbom, P. and Lamb, C.J. (1992) Elicitor-and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel rapid defense response. Cell 70: 21-30.
15. Breusegem, F.V. and Dat, J.F. (2006) Reactive oxygen species in plant cell death. Plant Physiol. 141: 384-390. (Pubitemid 43974532)
16. Brioudes, F., Thierry, A.M., Chambrier, P., Mollereau, B. and Bendahmane, M. (2010) Translationally controlled tumor protein is a conserved mitotic growth integrator in animals and plants. Proc. Natl Acad. Sci. USA 107: 16384-16389.
17. Brisson, L.F., Tenhaken, R. and Lamb, C.J. (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6: 1703-1712. (Pubitemid 24986948)
18. Chakravarthy, S., Velásquez, A.C. and Martin, G.B. (2009) Assay for pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) in plants. J. Vis. Exp. 31: 1442.
19. del Pozo, O. and Lam, E. (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Cur. Biol. 8: 1129-1132. (Pubitemid 28501377)
20. Dickman, M.B., Park, Y.K., Oltersdorf, T., Li, W., Clemente, T. and French, R. (2001) Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc. Natl Acad. Sci. USA 98: 6957-6962. (Pubitemid 32538324)
21. Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A. and Dangl, J.L. (1994) Arabidopsis mutants simulating disease resistance response. Cell 77: 565-577. (Pubitemid 24153996)
22. - generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiol. Plant Pathol. 27: 311-322.
23. Ekengren, S.K., Liu, Y., Schiff, M., Dinesh-Kumar, S.P. and Martin, G.B. (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 36: 905-917. (Pubitemid 38069776)
24. Evan, G. and Littlewood, T. (1998) A matter of life and cell death. Science 281: 1317-1322. (Pubitemid 28406818)
25. Gechev, T.S. and Hille, J. (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. J. Cell. Sci 168: 17-20. (Pubitemid 40111052)
26. Gilchrist, D.G. (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu. Rev. Phytopathol. 36: 393-414. (Pubitemid 28456414)
27. Gnanasekar, M., Thirugnanam, S., Zheng, G., Chen, A. and Ramaswamy, K. (2009) Gene silencing of translationally controlled tumor protein (TCTP) by siRNA inhibits cell growth and induces apoptosis of human prostate cancer cells. Int. J. Oncol. 34: 1241-1246.
28. Gohre, V. and Robatzek, S. (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu. Rev. Phytopathol. 46: 189-215.
29. Greenberg, J.T. (1996) Programmed cell death: a way of life for plants. Proc. Natl Acad. Sci. USA 93: 12094-12097. (Pubitemid 26367100)
30. Greenberg, J.T. and Yao, N. (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol. 6: 201-211. (Pubitemid 38248004)
31. Groom, Q.J., Torres, M.A., Fordham-Skelton, A.P., Hammond-Kosack, K.E., Robinson, N.J. and Jones, J.D.G. (1996) RbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J. 10: 515-522. (Pubitemid 27108404)
32. Huitema, E., Vleeshouwers, V.G.A.A., Cakir, C., Kamoun, S. and Govers, F. (2005) Differences in intensity and specificity of hypersensitive response induction in Nicotiana spp. by INF1, INF2A, and INF2B of Phytophthora infestans. Mol. Plant-Microbe Interact 18: 183-193. (Pubitemid 40263613)
33. Jabs, T., Dietrich, R.A. and Dangl, J.L. (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273: 1853-1856. (Pubitemid 26322494)
34. Jin, H., Liu, Y., Yang, K.Y., Kim, C.Y., Baker, B. and Zhang, S. (2003) Function of mitogen-activated protein kinase pathway in N genemediated resistance in tobacco. Plant J. 33: 719-731. (Pubitemid 36325914)
35. Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS function: b-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 901-907.
36. Jones, J.D. and Dangl, J.L. (2006) The plant immune system. Nature 444: 323-329. (Pubitemid 44764102)
37. Kato, H., Asai, S., Yamamoto-Katou, A., Yoshioka, H., Doke, N. and Kawakita, K. (2008) Involvement of NbNOA1 in NO production and defense responses in INF1-treated Nicotiana benthamiana. J. Gen. Plant Pathol. 74: 15-23. (Pubitemid 351170153)
38. Katou, S., Yamamoto, A., Yoshioka, H., Kawakita, K. and Doke, N. (2003) Functional analysis of potato mitogen-activated protein kinase kinase, StMEK1. J. Gen. Plant Pathol. 69: 161-168.
39. Kiba, A., Maimbo, M., Kanda, A., Tomiyama, H., Ohnishi, K. and Hikichi, Y. (2007) Isolation and expression analysis of candidate genes related to Ralstonia solanacearum-tobacco interaction. Plant Biotechnol. 24: 409-416. (Pubitemid 47451006)
40. Kiba, A., Nakano, M., Vincent-Pope, P., Takahashi, H., Sawasaki, T., Endo, Y. et al. (2012) A novel Sec14 phospholipid transfer protein from Nicotiana benthamiana is up-regulated in response to Ralstonia solanacearum infection, pathogen associated molecular patterns and effector molecules and involved in plant immunity. J. Plant Physiol. 169: 1017-1022.
41. Kiba, A., Sangawa, Y., Ohnishi, K., Yao, N., Park, P.Y., Nakayashiki, H. et al. (2006a) Induction of apoptotic cell death leads to the development of bacterial rot caused by Pseudomonas cichorii. Mol. Plant-Microbe Interact. 19: 112-122. (Pubitemid 43172825)
42. Kiba, A., Takata, O., Ohnishi, K. and Hikichi, Y. (2006b) Comparative analysis of induction pattern of programmed cell death and defense-related responses during hypersensitive cell death and development of bacterial necrotic leaf spots in eggplant. Planta 224: 981-994. (Pubitemid 44435849)
43. Kiba, A., Tomiyama, H., Takahashi, H., Hamada, H., Ohnishi, K., Okuno, T. et al. (2003) Induction of resistance and expression of defense-related genes in tobacco leaves infiltrated with Ralstonia solanacearum. Plant Cell Physiol. 44: 287-295. (Pubitemid 36439864)
44. Kobayashi, M., Ohura, I., Kawakita, K., Yokota, N., Fujiwara, M., Shimamoto, K. et al. (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19: 1065-1080. (Pubitemid 46953247)
45. Komori, D., Nishihara, M., Takahashi, A., Gupta, M., Yoshioka, H., Mizumoto, H. et al. (2012) Isolation and characterization of an asparagine-rich protein that regulates hypersensitive cell death-mediated resistance in Nicotiana plants. Plant Biotechnol. 29: 293-300.
46. Kuc, J. (1972) Phytoalexins. Annu. Rev. Phytopathol. 10: 207-232.
47. Lacomme, C. and Santa-Cruz, S. (1999) Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl Acad. Sci. USA 96: 7956-7961. (Pubitemid 29328389)
48. Lam, E. (2004) Controlled cell death, plant survival and development. Nat. Rev. Mol. Cell Biol. 5: 305-315. (Pubitemid 38480611)
49. Lam, E., Kato, N. and Lawton, M. (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 848-853. (Pubitemid 32588113)
50. Maimbo, M., Ohnishi, K., Hikichi, Y., Yoshioka, H. and Kiba, A. (2007) Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solana-cearum. Plant Physiol. 145: 1588-1599. (Pubitemid 350276778)
51. Maimbo, M., Ohnishi, K., Hikichi, Y., Yoshioka, H. and Kiba, A. (2010) S glycoprotein-like protein regulates defense responses in Nicotiana plants against Ralstonia solanacearum. Plant Physiol. 152: 2023-2035.
52. Mauch, F. and Staehelin, A. (1989) Functional implications of the subcellular localization of ethylene-induced chitinase and b-1, 3 glu-canase in bean leaves. Plant Cell 1: 447-457.
53. Mitsuhara, I., Malik, K.A., Miura, M. and Ohashi, Y. (1999) Animal cell-death suppressors Bcl-x(L) and Ced-9 inhibit cell death in tobacco plants. Curr. Biol. 9: 775-778. (Pubitemid 29350860)
54. Nürnberger, T., Brunner, F., Kemmerling, B. and Piater, L. (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198: 249-266. (Pubitemid 38406948)
55. Ohta, S., Mita, A., Hattori, T. and Nakamura, K. (1990) Construction and expression in tobacco of a b-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol. 31: 805-813.
56. Pontier, D., Godiard, L., Marco, Y. and Roby, D. (1994) hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J. 5: 507-521.
57. Pontier, D., Tronchet, M., Rogowsky, P., Lam, E. and Roby, D. (1998) Activation of hsr203J, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol. Plant-Microbe Interact. 11: 544-554. (Pubitemid 28244579)
58. Poueymiro, M., Cunnac, S., Barberis, P., Deslandes, L., Peeters, N., Cazale-Noel, A.C. et al. (2010) Two type III secretion system effectors from Ralstonia solanacearum GMI1000 determine hostrange specificity on tobacco. Mol. Plant-Microbe. Interact. 22: 538-550.
59. Rodriguez, M.C.S., Pertersen, M. and Mundy, J. (2010) Mitogen-activated protein kinase in plants. Annu. Rev. Plant Biol. 61: 621-649.
60. Tomita, R., Sekine, K., Mizumoto, H., Sakamoto, M., Murai, J., Kiba, A. et al. (2010) Genetic basis for the hierarchical interaction between Tobamovirus spp. and L resistance gene alleles from different pepper species. Mol. Plant-Microbe Interact 24: 108-117.
61. Torres, M.A., Dangl, J.L. and Jones, J.D. (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA 99: 517-522. (Pubitemid 34060393)
62. Vance, C.P., Kink, I.K. and Sherwood, R.T. (1980) Lignification as a mechanism of disease resistance. Annu. Rev. Phytopathol. 18: 259-288.
63. Woo, H.H. and Hawes, M.C. (1997) Cloning of genes whose expression is correlated with mitosis and localized in dividing cells in root caps of Pisum sativum L. Plant Mol. Biol. 35: 1045-1051. (Pubitemid 28016966)
64. Xu., P., Rogers, S.J. and Roossinck, M.J. (2004) Expression of antiapop-totic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress. Proc. Natl Acad. Sci. USA 101: 15805-15810. (Pubitemid 39473569)
65. Yang, Y., Yang, F., Xiong, Z., Yan, Y., Wang, X., Nishino, M. et al. (2005) An N-terminal region of translationally controlled tumor protein is required for its antiapoptotic activity. Oncogene 24: 4778-4788. (Pubitemid 41076295)
66. Yoshioka, H., Asai, S., Yoshioka, M. and Kobayashi, M. (2009) Molecular mechanisms of generation for nitric oxide and reactive oxygen species, and role of the radical burst in plant immunity. Mol. Cell 28: 321-329.
67. 2 accumulation and resistance to Phytophthora infestans. Plant Cell 15: 706-718. (Pubitemid 36339583)
68. Zipfel, C. (2008) Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20: 10-16.