TGBp3 triggers the unfolded protein response and SKP1-dependent programmed cell death

Molecular Plant Pathology

Volumn 14, Issue 3, 2013, Pages 241-255

  Ye, Chang Ming ^a   Chen, Shaorong ^b   Payton, Mark ^a   Dickman, Martin B ^b   Verchot, Jeanmarie ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VEGETABLE PROTEIN; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; GENETICS; METABOLISM; PHYSIOLOGY; POTEXVIRUS; TOBACCO MOSAIC VIRUS; TRANSGENIC PLANT; UNFOLDED PROTEIN RESPONSE;

APOPTOSIS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POTEXVIRUS; TOBACCO MOSAIC VIRUS; UNFOLDED PROTEIN RESPONSE; VIRAL PROTEINS;

EID: 84874730049     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12000     Document Type: Article

References (91)

1. Aronson, M.N., Meyer, A.D., Gyorgyey, J., Katul, L., Vetten, H.J., Gronenborn, B. and Timchenko, T. (2000) Clink, a nanovirus-encoded protein, binds both pRB and SKP1. J. Virol. 74, 2967-2972.
2. Azevedo, C., Betsuyaku, S., Peart, J., Takahashi, A., Noel, L., Sadanandom, A., Casais, C., Parker, J. and Shirasu, K. (2006) Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J. 25, 2007-2016.
3. Bhattarai, K.K., Li, Q., Liu, Y., Dinesh-Kumar, S.P. and Kaloshian, I. (2007) The MI-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol. 144, 312-323.
4. Carette, J.E., Stuiver, M., Van Lent, J., Wellink, J. and Van Kammen, A. (2000) Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on denovo membrane synthesis. J. Virol. 74, 6556-6563.
5. Carette, J.E., van Lent, J., MacFarlane, S.A., Wellink, J. and van Kammen, A. (2002) Cowpea mosaic virus 32- and 60-kilodalton replication proteins target and change the morphology of endoplasmic reticulum membranes. J. Virol. 76, 6293-6301.
6. Chae, H.J., Ke, N., Kim, H.R., Chen, S., Godzik, A., Dickman, M. and Reed, J.C. (2003) Evolutionarily conserved cytoprotection provided by Bax Inhibitor-1 homologs from animals, plants, and yeast. Gene, 323, 101-113.
7. Chen, S., Vaghchhipawala, Z., Li, W., Asard, H. and Dickman, M.B. (2004) Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol. 135, 1630-1641.
8. Chen, S.R., Dunigan, D.D. and Dickman, M.B. (2003) Bcl-2 family members inhibit oxidative stress-induced programmed cell death in Saccharomyces cerevisiae. Free Radic. Biol. Med. 34, 1315-1325.
9. Cheng, Y.T., Li, Y., Huang, S., Huang, Y., Dong, X., Zhang, Y. and Li, X. (2011) Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc. Natl. Acad. Sci. USA, 108, 14694-14699.
10. Costa, M.D., Reis, P.A., Valente, M.A., Irsigler, A.S., Carvalho, C.M., Loureiro, M.E., Aragão, F.J., Boston, R.S., Fietto, L.G. and Fontes, E.P. (2008) A new branch of endoplasmic reticulum stress signaling and the osmotic signal converge on plant-specific asparagine-rich proteins to promote cell death. J. Biol. Chem. 283, 20209-20219.
11. Crosti, P., Malerba, M. and Bianchetti, R. (2001) Tunicamycin and brefeldin A induce in plant cells a programmed cell death showing apoptotic features. Protoplasma, 216, 31-38.
12. Denecke, J., Goldman, M.H., Demolder, J., Seurinck, J. and Botterman, J. (1991) The tobacco luminal binding protein is encoded by a multigene family. Plant Cell, 3, 1025-1035.
13. Denecke, J., Carlsson, L.E., Vidal, S., Hoglund, A.S., Ek, B., van Zeijl, M.J., Sinjorgo, K.M. and Palva, E.T. (1995) The tobacco homolog of mammalian calreticulin is present in protein complexes invivo. Plant Cell, 7, 391-406.
14. Deng, Y., Humbert, S., Liu, J.X., Srivastava, R., Rothstein, S.J. and Howell, S.H. (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc. Natl. Acad. Sci. USA, 108, 7247-7252.
15. 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.
16. Ellgaard, L. and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191.
17. Erickson, F.L., Dinesh-Kumar, S.P., Holzberg, S., Ustach, C.V., Dutton, M., Handley, V., Corr, C. and Baker, B.J. (1999) Interactions between Tobacco mosaic virus and the tobacco N gene. Philos. Trans. R. Soc. London: B. Biol. Sci. 354, 653-658.
18. Gfeller, A., Liechti, R. and Farmer, E.E. (2010) Arabidopsis jasmonate signaling pathway. Sci. Signal 3, cm4.
19. 2+/calmodulin-dependent signalling pathway is responsible for the resistance of Arabidopsis dnd1 against Pectobacterium carotovorum infection. Mol. Plant Pathol. 8, 747-759.
20. Iwata, Y. and Koizumi, N. (2005a) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc. Natl. Acad. Sci. USA, 102, 5280-5285.
21. Iwata, Y. and Koizumi, N. (2005b) Unfolded protein response followed by induction of cell death in cultured tobacco cells treated with tunicamycin. Planta, 220, 804-807.
22. Iwata, Y. and Koizumi, N. (2012) Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci. (Available at http://dx.doi.org/10.1016/j.tplants.2012.06.014).
23. Iwata, Y., Yoneda, M., Yanagawa, Y. and Koizumi, N. (2009) Characteristics of the nuclear form of the Arabidopsis transcription factor AtbZIP60 during the endoplasmic reticulum stress response. Biosci. Biotechnol. Biochem. 73, 865-869.
24. Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
25. Jelitto-Van Dooren, E.P., Vidal, S. and Denecke, J. (1999) Anticipating endoplasmic reticulum stress. A novel early response before pathogenesis-related gene induction. Plant Cell, 11, 1935-1944.
26. Ju, H.J., Samuels, T.D., Wang, Y.S., Blancaflor, E., Payton, M., Mitra, R., Krishnamurthy, K., Nelson, R.S. and Verchot-Lubicz, J. (2005) The potato virus X TGBp2 movement protein associates with endoplasmic reticulum-derived vesicles during virus infection. Plant Physiol. 138, 1877-1895.
27. Ju, H.J., Ye, C.M. and Verchot-Lubicz, J. (2008) Mutational analysis of Potato virus X TGBp3 links subcellular accumulation to protein turnover during virus infection. Virology, 375, 103-117.
28. Kadota, Y., Amigues, B., Ducassou, L., Madaoui, H., Ochsenbein, F., Guerois, R. and Shirasu, K. (2008) Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Rep. 9, 1209-1215.
29. Kamauchi, S., Nakatani, H., Nakano, C. and Urade, R. (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J. 272, 3461-3476.
30. Khanna, H.K., Paul, J.Y., Harding, R.M., Dickman, M.B. and Dale, J.L. (2007) Inhibition of Agrobacterium-induced cell death by antiapoptotic gene expression leads to very high transformation efficiency of banana. Mol. Plant-Microbe Interact. 20, 1048-1054.
31. Kim, K.S., Min, J.Y. and Dickman, M.B. (2008) Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol. Plant-Microbe Interact. 21, 605-612.
32. Koizumi, N., Ujino, T., Sano, H. and Chrispeels, M.J. (1999) Overexpression of a gene that encodes the first enzyme in the biosynthesis of asparagine-linked glycans makes plants resistant to tunicamycin and obviates the tunicamycin-induced unfolded protein response. Plant Physiol. 121, 353-361.
33. Lam, E. (2005) Vacuolar proteases livening up programmed cell death. Trends Cell Biol. 15, 124-127.
34. Leborgne-Castel, N., Jelitto-Van Dooren, E.P., Crofts, A.J. and Denecke, J. (1999) Overexpression of BiP in tobacco alleviates endoplasmic reticulum stress. Plant Cell, 11, 459-470.
35. Lee, W.M. and Ahlquist, P. (2003) Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J. Virol. 77, 12819-12828.
36. Lindbo, J.A. (2007a) High-efficiency protein expression in plants from agroinfection-compatible Tobacco mosaic virus expression vectors. BMC Biotechnol. 7, 52-63.
37. Lindbo, J.A. (2007b) TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol. 145, 1232-1240.
38. Liu, J.X., Srivastava, R., Che, P. and Howell, S.H. (2007) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell, 19, 4111-4119.
39. Liu, Y., Schiff, M., Serino, G., Deng, X.W. and Dinesh-Kumar, S.P. (2002) Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to Tobacco mosaic virus. Plant Cell, 14, 1483-1496.
40. Liu, Y., Burch-Smith, T., Schiff, M., Feng, S. and Dinesh-Kumar, S.P. (2004) Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 279, 2101-2108.
41. Liu, Z. and Kearney, C.M. (2010) A tobamovirus expression vector for agroinfection of legumes and Nicotiana. J. Biotechnol. 147, 151-159.
42. Lu, D.P. and Christopher, D.A. (2008) Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol. Genet. Genomics, 280, 199-210.
43. Mahalingam, R., Jambunathan, N., Gunjan, S.K., Faustin, E., Weng, H. and Ayoubi, P. (2006) Analysis of oxidative signalling induced by ozone in Arabidopsis thaliana. Plant Cell Environ. 29, 1357-1371.
44. Malerba, M., Cerana, R. and Crosti, P. (2004) Comparison between the effects of fusicoccin, tunicamycin, and brefeldin A on programmed cell death of cultured sycamore (Acer pseudoplatanus L.) cells. Protoplasma, 224, 61-70.
45. Malerba, M., Contran, N., Tonelli, M., Crosti, P. and Cerana, R. (2008) Role of nitric oxide in actin depolymerization and programmed cell death induced by fusicoccin in sycamore (Acer pseudoplatanus) cultured cells. Physiol. Plant. 133, 449-457.
46. Malim, M.H. and Emerman, M. (2008) HIV-1 accessory proteins-ensuring viral survival in a hostile environment. Cell Host Microbe, 3, 388-398.
47. Martinez, I.M. and Chrispeels, M.J. (2003) Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell, 15, 561-576.
48. Meusser, B., Hirsch, C., Jarosch, E. and Sommer, T. (2005) ERAD: the long road to destruction. Nat. Cell Biol. 7, 766-772.
49. Muller, J., Piffanelli, P., Devoto, A., Miklis, M., Elliott, C., Ortmann, B., Schulze-Lefert, P. and Panstruga, R. (2005) Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell, 17, 149-163.
50. 2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol. 125, 2129-2138.
51. Netherton, C., Moffat, K., Brooks, E. and Wileman, T. (2007) A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv. Virus Res. 70, 101-182.
52. Nomaguchi, M., Fujita, M. and Adachi, A. (2008) Role of HIV-1 Vpu protein for virus spread and pathogenesis. Microbes Infect. 10, 960-967.
53. Oh, D.H., Kwon, C.S., Sano, H., Chung, W.I. and Koizumi, N. (2003) Conservation between animals and plants of the cis-acting element involved in the unfolded protein response. Biochem. Biophys. Res. Commun. 301, 225-230.
54. Parmar, V.M. and Schroder, M. (2012) Sensing endoplasmic reticulum stress. Adv. Exp. Med. Biol. 738, 153-168.
55. Pazhouhandeh, M., Dieterle, M., Marrocco, K., Lechner, E., Berry, B., Brault, V., Hemmer, O., Kretsch, T., Richards, K.E., Genschik, P. and Ziegler-Graff, V. (2006) F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc. Natl. Acad. Sci. USA, 103, 1994-1999.
56. Pike, S.M., Zhang, X.C. and Gassmann, W. (2005) Electrophysiological characterization of the Arabidopsis avrRpt2-specific hypersensitive response in the absence of other bacterial signals. Plant Physiol. 138, 1009-1017.
57. Qiang, X., Zechmann, B., Reitz, M.U., Kogel, K.H. and Schafer, P. (2012) The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell, 24, 794-809.
58. Ren, C., Pan, J., Peng, W., Genschik, P., Hobbie, L., Hellmann, H., Estelle, M., Gao, B., Peng, J., Sun, C. and Xie, D. (2005) Point mutations in Arabidopsis Cullin1 reveal its essential role in jasmonate response. Plant J. 42, 514-524.
59. Ritzenthaler, C., Laporte, C., Gaire, F., Dunoyer, P., Schmitt, C., Duval, S., Piéquet, A., Loudes, A.M., Rohfritsch, O., Stussi-Garaud, C. and Pfeiffer, P. (2002) Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J. Virol. 76, 8808-8819.
60. Roberts, M.R. and Bowles, D.J. (1999) Fusicoccin, 14-3-3 proteins, and defense responses in tomato plants. Plant Physiol. 119, 1243-1250.
61. Schaad, M.C., Jensen, P.E. and Carrington, J.C. (1997) Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J. 16, 4049-4059.
62. Schott, A., Ravaud, S., Keller, S., Radzimanowski, J., Viotti, C., Hillmer, S., Sinning, I. and Strahl, S. (2010) Arabidopsis stromal-derived Factor2 (SDF2) is a crucial target of the unfolded protein response in the endoplasmic reticulum. J. Biol. Chem. 285, 18113-18121.
63. Schubert, U., Anton, L.C., Bacik, I., Cox, J.H., Bour, S., Bennink, J.R., Orlowski, M., Strebel, K. and Yewdell, J.W. (1998) CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. J. Virol. 72, 2280-2288.
64. Seo, P.J., Kim, S.G. and Park, C.M. (2008) Membrane-bound transcription factors in plants. Trends Plant Sci. 13, 550-556.
65. Shadwick, F.S. and Doran, P.M. (2007) Propagation of plant viruses in hairy root cultures: a potential method for invitro production of epitope vaccines and foreign proteins. Biotechnol. Bioeng. 96, 570-583.
66. Sharma, M., Sasvari, Z. and Nagy, P.D. (2011) Inhibition of phospholipid biosynthesis decreases the activity of the tombusvirus replicase and alters the subcellular localization of replication proteins. Virology, 415, 141-152.
67. Shivprasad, S., Pogue, G.P., Lewandowski, D.J., Hidalgo, J., Donson, J., Grill, L.K. and Dawson, W.O. (1999) Heterologous sequences greatly affect foreign gene expression in tobacco mosaic virus-based vectors. Virology, 255, 312-323.
68. Slepak, T.I., Tang, M., Slepak, V.Z. and Lai, K. (2007) Involvement of endoplasmic reticulum stress in a novel Classic Galactosemia model. Mol. Genet. Metab. 92, 78-87.
69. Smalle, J. and Vierstra, R.D. (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590.
70. Stuttmann, J., Lechner, E., Guerois, R., Parker, J.E., Nussaume, L., Genschik, P. and Noël, L.D. (2009) COP9 signalosome- and 26S proteasome-dependent regulation of SCFTIR1 accumulation in Arabidopsis. J. Biol. Chem. 284, 7920-7930.
71. Su, W., Liu, Y., Xia, Y., Hong, Z. and Li, J. (2011) Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. Proc. Natl. Acad. Sci. USA, 108, 870-875.
72. Tabas, I. and Ron, D. (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13, 184-190.
73. Tardif, K.D., Mori, K., Kaufman, R.J. and Siddiqui, A. (2004) Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J. Biol. Chem. 279, 17158-17164.
74. Tateda, C., Ozaki, R., Onodera, Y., Takahashi, Y., Yamaguchi, K., Berberich, T., Koizumi, N. and Kusano, T. (2008) NtbZIP60, an endoplasmic reticulum-localized transcription factor, plays a role in the defense response against bacterial pathogens in Nicotiana tabacum. J. Plant Res. 121, 603-611.
75. Thiel, H., Hleibieh, K., Gilmer, D. and Varrelmann, M. (2012) The P25 pathogenicity factor of Beet necrotic yellow vein virus targets the sugar beet 26S proteasome involved in the induction of a hypersensitive resistance response via interaction with an F-box protein. Mol. Plant-Microbe Interact. 25, 1058-1072.
76. Turner, K.A., Sit, T.L., Callaway, A.S., Allen, N.S. and Lommel, S.A. (2004) Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology, 320, 276-290.
77. Urade, R. (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J. 274, 1152-1171.
78. Verchot, J. (2011) Wrapping membranes around plant virus infection. Curr. Opin. Virol. 1, 388-395.
79. Verchot, J., Angell, S.M. and Baulcombe, D.C. (1998) Invivo translation of the triple gene block of potato virus X requires two subgenomic mRNAs. J. Virol. 72, 8316-8320.
80. Watanabe, N. and Lam, E. (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J. 45, 884-894.
81. Watanabe, N. and Lam, E. (2008a) Arabidopsis Bax inhibitor-1: a rheostat for ER stress-induced programmed cell death. Plant Signal Behav. 3, 564-566.
82. Watanabe, N. and Lam, E. (2008b) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J. Biol. Chem. 283, 3200-3210.
83. Williams, B.L. and Lipkin, W.I. (2006) Endoplasmic reticulum stress and neurodegeneration in rats neonatally infected with borna disease virus. J. Virol. 80, 8613-8626.
84. Xu, C., Bailly-Maitre, B. and Reed, J.C. (2005) Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115, 2656-2664.
85. Xu, L., Liu, F., Lechner, E., Genschik, P., Crosby, W.L., Ma, H., Peng, W., Huang, D. and Xie, D. (2002) The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell, 14, 1919-1935.
86. Xu, P., Rogers, S.J. and Roossinck, M.J. (2004) Expression of antiapoptotic 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.
87. Ye, C. and Verchot, J. (2011) Role of unfolded protein response in plant virus infection. Plant Signal Behav. 6, 1212-1215.
88. Ye, C., Dickman, M.B., Whitham, S.A., Payton, M. and Verchot, J. (2011) The unfolded protein response is triggered by a plant viral movement protein. Plant Physiol. 156, 741-755.
89. Ye, C.M., Kelly, V., Payton, M., Dickman, M.B. and Verchot, J. (2012) SGT1 is induced by the Potato virus X TGBp3 and enhances virus accumulation in Nicotiana benthamiana. Mol. Plant, 5, 1151-1153.
90. Zhang, K. and Kaufman, R.J. (2006) The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology, 66, S102-S109.
91. Zheng, X., Miller, N.D., Lewis, D.R., Christians, M.J., Lee, K.H., Muday, G.K., Spalding, E.P. and Vierstra, R.D. (2011) AUXIN UP-REGULATED F-BOX PROTEIN1 regulates the cross talk between auxin transport and cytokinin signaling during plant root growth. Plant Physiol. 156, 1878-1893.