Insights into Alternanthera mosaic virus TGB3 functions: Interactions with Nicotiana benthamiana PsbO correlate with chloroplast vesiculation and veinal necrosis caused by TGB3 over-expression

Frontiers in Plant Science

Volumn 4, Issue JAN, 2013, Pages

  Jang, Chanyong ^a   Seo, Eun Young ^a   Nam, Jiryun ^a   Bae, Hanhong ^b   Gim, Yeong Guk ^a   Kim, Hong Gi ^a   Cho, In Sook ^c   Lee, Zee Won ^d   Bauchan, Gary R ^e   Hammond, John ^e   Lim, Hyoun Sub ^a  

^a Chungnam National University   (South Korea)

^b Yeungnam University   (South Korea)

^c Rural Development Administration   (South Korea)

^d Korea Basic Science Institute (KBSI)   (South Korea)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

AltMV; Chloroplast; Potexvirus; PsbO; TGB3

Indexed keywords

EID: 84899146540     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00005     Document Type: Article

References (82)

1. Abbink, T. E., Peart, J. R., Mos, T. N., Baulcombe, D. C., Bol, J. F., and Linthorst, H. J. (2002). Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants. Virology 295, 307-319.
2. Bamunusinghe, D., Hemenway, C. L., Nelson, R. S., Sanderfoot, A. A., Ye, C. M., Silva, M. A. T., et al. (2009). Analysis of potato virus X replicase and TGBp3 subcellular locations. Virology 393, 272-285.
3. Beck, D. L., Guilford, P. J., Voot, D. M., Andersen, M. T., and Forster, R. L. (1991). Triple gene block proteins of white clover mosaic potexvirus are required for transport. Virology 183, 695-702.
4. Becker, D. M., Fikes, J. D., and Guarente, L. (1991). A cDNA encoding a human CCAAT-binding protein cloned by functional complementation in yeast. Proc. Natl. Acad. Sci. U.S.A. 88, 1968-1972.
5. Bragg, J. N., and Jackson, A. O. (2004). The C-terminal region of the Barley stripe mosaic virus gamma b protein participates in homologous interactions and is required for suppression of RNA silencing. Mol. Plant Pathol. 5, 465-481.
6. Bricker, T. M., Roose, J. L., Fagerlund, R. D., Frankel, L. K., and Eaton-Rye, J. J. (2012). The extrinsic proteins of Photosystem II. Biochim. Biophys. Acta 1817, 121-142.
7. 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 de novomembrane synthesis. J. Virol. 74, 6556-6563.
8. Chalcroft, J., and Matthews, R. E. (1966). Cytological changes induced by turnip yellow mosaic virus in Chinese cabbage leaves. Virology 28, 555-562.
9. Cheng, Y. Q., Liu, Z. M., Xu, J., Zhou, T., Wang, M., Chen, Y. T., et al. (2008). HC-Pro protein of sugar cane mosaic virus interacts specifically with maize ferredoxin-5 in vitro and in planta. J. Gen. Virol. 89, 2046-2054.
10. Cowan, G. H., Lioliopoulou, F., Ziegler, A., and Torrance, L. (2002). Subcellular localisation, protein interactions, and RNA binding of Potato mop-top virus triple gene block proteins. Virology 298, 106-115.
11. Dardick, C. (2007). Comparative expression profiling of Nicotiana benthamiana leaves systemically infected with three fruit tree viruses. Mol. Plant Microbe Interact. 20, 1004-1017.
12. Davies, C., Hills, G., and Baulcombe, D. C. (1993). Sub-cellular localization of the 25-kDa protein encoded in the triple gene block of potato virus X. Virology 197, 166-175.
13. Deng, M., Bragg, J. N., Ruzin, S., Schichnes, D., King, D., Goodin, M. M., et al. (2007). Role of the sonchus yellow net virus N protein in formation of nuclear viroplasms. J. Virol. 81, 5362-5374.
14. Esau, K., and Cronshaw, J. (1967). Relation of tobacco mosaic virus to the host cells. J. Cell Biol. 33, 665-678.
15. Feki, S., Loukili, M. J., Triki-Marrakchi, R., Karimova, G., Old, I., Ounouna, H., et al. (2005). Interaction between tobacco Ribulose-l,5-biphosphate Carboxylase/Oxygenase large subunit (RubisCO-LSU) and the PVY Coat Protein (PVY-CP). Eur. J. Plant Pathol. 112, 221-234.
16. Genoud, T., Buchala, A. J., Chua, N. H., and Métraux, J. P. (2002). Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. Plant J. 31, 87-95.
17. Goodin, M. M., Dietzgen, R. G., Schichnes, D., Ruzin, S., and Jackson, A. O. (2002). pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J. 31, 375-383.
18. Granett, A. L., and Shalla, T. A. (1970). Discrepancies in the intracellular behavior of three strains of tobacco mosaic virus, two of which are serologically indistinguishable. Phytopathology 60, 419-425.
19. Grangeon, R., Agbeci, M., Chen, J., Grondin, G., Zheng, H., and Laliberté, J. F. (2012). Impact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection. J. Virol. 86, 9255-9265.
20. Griebel, T., and Zeier, J. (2008). Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol.147, 790-801.
21. Gunasinghe, U. B., and Berger, P. H. (1991). Association of potato virus Y gene products with chloroplasts in tobacco. Mol. Plant Microbe Interact. 4, 452-457.
22. Hammond, J., Reinsel, M. D., and Maroon-Lango, C. J. (2006a). Identification and full sequence of an isolate of Alternanthera mosaic potexvirus infecting Phlox stolonifera. Arch. Virol. 151, 477-493.
23. Hammond, J., Reinsel, M. D., and Maroon-Lango, C. J. (2006b). Identification of potexvirus isolates from phlox and portulaca as strains of Alternanthera mosaic virus. Acta Hortic. 722, 71-77.
24. Holmes, F. O. (1931). Local lesions of mosaic in Nicotiana tabacum L. Contrib. Boyce Thompson Inst. 3, 163-172.
25. Ivanov, P. A., Mukhamedzhanova, A. A., Smirnov, A. A., Rodionova, N. P., Karpova, O. G., and Atebekov, J. G. (2011). The complete nucleotide sequence of Alternanthera mosaic virus infecting Portulaca grandiflora represents a new strain distinct from phlox isolates. Virus Genes 42, 268-271.
26. Jiménez, I., López, L., Alamillo, J. M., Valli, A., and García, J. A. (2006). Identification of a plum pox virus CI-interacting protein from chloroplast that has a negative effect in virus infection. Mol. Plant Microbe Interact. 19, 350-358.
27. Jin, Y., Ma, D., Dong, J., Li, D., Deng, C., Jin, J., et al. (2007). The HC-pro protein of potato virus Y interacts with NtMinD of tobacco. Mol. Plant Microbe Interact. 20, 1505-1511.
28. Johansen, L. K., and Carrington, J. C. (2001). Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 126, 930-938.
29. Ju, H. J., Samuels, T. D., Wang, Y. S., Blancaflor, E., Payton, M., Mitra, R., et al. (2005). The potato virus X TGBp2 movement protein associates with endoplasmic reticulum-derived vesicles during virus infection. Plant Physiol.138, 1877-1895.
30. Ju, H. J., Ye, C. M., and Verchot-Lubicz, J. (2008). Mutational analysis of PVX TGBp3 links subcellular accumulation and protein turnover. Virology 375, 103-117.
31. Lawrence, S. D., and Kindle, K. L. (1997). Alterations in the Chlamydomonas plastocyanin transit peptide have distinct effects on in vitro import and in vivo protein accumulation. J. Biol. Chem. 272, 20357-20363.
32. Lawson, R. H., and Hearon, S. S. (1973). Ultrastructure of Carnation etched ring virus-infected Saponaria vaccaria and Dianthus caryophyllus. J. Ultrastruct. Res. 48, 201-215.
33. Lee, S. C., Wu, C. H., and Wang, C. W. (2010). Traffic of a viral movement protein complex to the highly curved tubules of the cortical endoplasmic reticulum. Traffic 11, 912-930.
34. Lehto, K., Tikkanen, M., Hiriart, J. B., Paakkarinen, V., and Aro, E. M. (2003). Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus. Mol. Plant Microbe Interact. 16, 1135-1144.
35. Lim, H. S., Bragg, J. N., Ganesan, U., Lawrence, D. M., Yu, J., Isogai, M., et al. (2008). Triple gene block protein interactions involved in movement of Barley stripe mosaic virus. J. Virol. 82, 4991-5006.
36. Lim, H. S., Bragg, J. N., Ganesan, U., Ruzin, S., Schichnes, D., Lee, M. Y., et al. (2009). Subcellular localization of the Barley Stripe Mosaic Virus Triple Gene Block proteins. J. Virol. 83, 9432-9448.
37. Lim, H.-S., Vaira, A. M., Bae, H., Bragg, J. N., Ruzin, S. E., Bauchan, G. R., et al. (2010a). Mutation of a chloroplast targeting signal in Alternanthera mosaic virus TGB3 impairs cell-to-cell movement and eliminates long distance virus movement. J. Gen. Virol. 91, 2102-2115.
38. Lim, H.-S., Vaira, A. M., Reinsel, M. D., Bae, H., Bailey, B. A., Domier, L. L., et al. (2010b). Pathogenicity of Alternanthera mosaic virus pathogenicity is affected by determinants in RNA-dependent RNA polymerase and by reduced efficacy of silencing suppression in a movement-competent TGB1. J. Gen. Virol. 91, 277-287.
39. Lim, H.-S., Vaira, A. M., Domier, L. L., Lee, S. C., Kim, H. G., and Hammond, J. (2010c). Efficiency of VIGS and gene expression in a novel bipartite potexvirus vector delivery system as a function of strength of TGB1 silencing suppression. Virology 402, 149-163.
40. Lin, J. W., Ding, M. P., Hsu, Y. H., and Tsai, C. H. (2007). Chloroplast phosphoglycerate kinase, a gluconeogenetic enzyme, is required for efficient accumulation of Bamboo mosaic virus. Nucleic Acids Res. 35, 424-432.
41. Lin, M. K., Hu, C. C., Lin, N. S., Chang, B. Y., and Hsu, Y. H. (2006). Movement of potexviruses requires species-specific interactions among the cognate triple gene block proteins, as revealed by a trans-complementation assay based on the bamboo mosaic virus satellite RNA-mediated expression system. J. Gen. Virol. 87, 1357-1367.
42. Lough, T. J., Netzler, N. E., Emerson, S. J., Sutherland, P., Carr, F., Beck, D. L., et al. (2000). Cell-to-cell movement of potexviruses: evidence for a ribonucleoprotein complex involving the coat protein and first triple gene block protein. Mol. Plant Microbe Interact. 13, 962-974.
43. Lundin, B., Hansson, M., Schoefs, B., Vener, A. V., and Spetea, C. (2007a). The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J. 49, 528-539.
44. Lundin, B., Thuswaldner, S., Shutova, T., Eshaghi, S., Samuelsson, G., Barber, J., et al. (2007b). Subsequent events to GTP binding by the plant PsbO protein: structural changes, GTP hydrolysis and dissociation from the photosystem II complex. Biochim. Biophys. Acta 1767, 500-508.
45. Lundin, B., Nurmi, M., Rojas-Stuetz, M., Aro, E. M., Adamska, I., and Spetea, C. (2008). Towards understanding the functional difference between the two PsbO isoforms in Arabidopsis thaliana-insights from phenotypic analyses of psbo knockout mutants. Photosyn. Res. 98, 405-414.
46. Manfre, A., Glenn, M., Nuñez, A., Moreau, R. A., and Dardick, C. (2011). Light quantity and photosystem function mediate host susceptibility to Turnip mosaic virus via a salicylic acid-independent mechanism. Mol. Plant Microbe Interact. 24, 315-327.
47. McClintock, K., Lamarre, A., Parsons, V., Laliberté, J. F., and Fortin, M. G. (1998). Identification of a 37 kDa plant protein that interacts with the turnip mosaic potyvirus capsid protein using anti-idiotypic-antibodies. Plant Mol. Biol. 37, 197-204.
48. Morozov, S. Y., and Solovyev, A. G. (2003). Triple gene block: modular design of a multifunctional machine for plant virus movement. J. Gen. Virol. 84, 1351-1366.
49. Murakami, R., Ifuku, K., Takabayashi, A., Shikanai, T., Endo, T., and Sato, F. (2005). Functional dissection of two Arabidopsis PsbO proteins: PsbO1 and PsbO2. FEBS J. 272, 2165-2175.
50. Nam, J., Jang, C., Li, M., Kim, H., Cho, S., Kim, H., et al. (2012). Alternanthera mosaic virus TGB1 interaction with chloroplast β ATPase is necessary for viral replication. Phytopathology 102(Suppl. 4),: S4.85.
51. Pérez-Bueno, M. L., Barón, M., and García-Luque, I. (2011). PsbO, PsbP, and PsbQ of photosystem II are encoded by gene families in Nicotiana benthamiana. Structure and functionality of their isoforms. Photosynthetica 49, 573-580.
52. Pérez-Bueno, M. L., Rahoutei, J., Sajnani, C., García-Luque, I., and Barón, M. (2004). Proteomic analysis of the oxygen-evolving complex of photosystem II under biotec stress: studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4, 418-425.
53. Petty, I. T., Hunter, B. G., Wei, N., and Jackson, A. O. (1989). Infectious barley stripe mosaic virus RNA transcribed in vitro from full-length genomic cDNA clones. Virology 171, 342-349.
54. Prod'Homme, D., Jakubiec, A., Tournier, V., Drugeon, G., and Jupin, I. (2003). Targeting of the turnip yellow mosaic virus 66K replication protein to the chloroplast envelope is mediated by the 140K protein. J. Virol. 77, 9124-9135.
55. Prod'Homme, D., Le Panse, S., Drugeon, G., and Jupin, I. (2001). Detection and subcellular localization of the turnip yellow mosaic virus 66K replication protein in infected cells. Virology 281, 88-101.
56. Qiao, Y., Li, H. F., Wong, S. M., and Fan, Z. F. (2009). Plastocyanin transit peptide interacts with Potato virus X coat protein, while silencing of plastocyanin reduces coat protein accumulation in chloroplasts and symptom severity in host plants. Mol. Plant Microbe Interact. 22, 1523-1534.
57. Rahoutei, J., García-Luque, I., and Barón, M. (2000). Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol. Plant. 110, 286-292.
58. Reinero, A., and Beachy, R. N. (1986). Association of TMV coat protein with chloroplast membranes in virus-infected leaves. Plant Mol. Biol. 6, 291-301.
59. Ritzenthaler, C., Laporte, C., Gaire, F., Dunoyer, P., Schmitt, C., Duval, S., et al. (2002). Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J. Virol. 76, 8808-8819.
60. Samuels, T. D., Ju, H. J., Ye, C. M., Motes, C. M., Blancaflor, E. B., and Verchot-Lubicz, J. (2007). Subcellular targeting and interactions among the Potato virus X TGB proteins. Virology 367, 375-389.
61. Schepetilnikov, M. V., Manske, U., Solovyev, A. G., Zamyatnin, A. A. Jr., Schiemann, J., and Morozov, S. Y. (2005). The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J. Gen. Virol. 86, 2379-2391.
62. Schoelz, J. E., and Zaitlin, M. (1989). Tobacco mosaic virus RNA enters chloroplasts in vivo. Proc. Natl. Acad. Sci. U.S.A. 86, 4496-4500.
63. Shi, Y., Chen, J., Hong, X., Chen, J., and Adams, M. J. (2007). A potyvirus P1 protein interacts with the Rieske Fe/S protein of its host. Mol. Plant Pathol. 8, 785-790.
64. Shimizu, T., Satoh, K., Kikuchi, S., and Omura, T. (2007). The repression of cell wall-and plastid-related genes and the induction of defense-related genes in rice plants infected with Rice dwarf virus. Mol. Plant Microbe Interact.20, 247-254.
65. Solovyev, A. G., Stroganova, T. A., Zamyatnin, A. A. Jr., Fedorkin, O. N., Schiemann, J., and Morozov, S. Y. (2000). Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virology 269, 113-127.
66. Sui, C., Fan, Z., Wong, S.-M., and Li, H. (2006). Cloning of cDNAs encoding the three subunits of oxygen evolving complex in Nicotiana benthamiana and gene expression changes in tobacco leaves infected with Tobacco mosaic virus. Physiol. Mol. Plant Pathol. 68, 61-68.
67. Takahashi, H., and Ehara, Y. (1992). Changes in the activity and the polypeptide composition of the oxygen-evolving complex in photosystem II of tobacco leaves infected with cucumber mosaic virus strain Y. Mol. Plant Microbe Interact. 5, 269-272.
68. Takahashi, H., Ehara, Y., and Hirano, H. (1991). A protein in the oxygen-evolving complex in the chloroplast is associated with symptom expression on tobacco leaves infected with cucumber mosaic virus strain Y. Plant Mol. Biol. 16, 689-698.
69. Tilsner, J., Linnik, O., Wright, K. M., Bell, K., Roberts, A. G., Lacomme, C., et al. (2012). The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol.158, 1359-1370.
70. Torrance, L., Cowan, G. H., Gillespie, T., Ziegler, A., and Lacomme, C. (2006). Barley stripe mosaic virus-encoded proteins triple-gene block 2 and gamma-b localize to chloroplasts in virus-infected monocot and dicot plants, revealing hitherto-unknown roles in virus replication. J. Gen. Virol. 87, 2403-2411.
71. Trebitsh, T., and Danon, A. (2001). Translation of chloroplast psbA mRNA is regulated by signals initiated by both photosystems II and I. Proc. Natl. Acad. Sci. U.S.A. 98, 12289-12294.
72. Tyagi, A., Hermans, J., Steppuhn, J., Jansson, C., Vater, F., and Herrmann, R. G. (1987). Nucleotide sequence of cDNA clones encoding the complete "33 kDa" precursor protein associated with the photosynthetic oxygen-evolving complex from spinach. Mol. Gen. Genet. 207, 288-293.
73. Ushiyama, R., and Matthews, R. E. (1970). The significance of chloroplast abnormalities associated with infection by turnip yellow mosaic virus. Virology 42, 293-303.
74. Vaira, A. M., Lim, H. S., Bauchan, G. R., Owens, R. A., Natilla, A., Dienelt, M. M., et al. (2012). Lolium latent virus (Alphaflexiviridae) coat proteins: expression and functions in infected plant tissue. J. Gen. Virol. 93, 1814-1824.
75. Verchot-Lubicz, J. (2005). A new cell-to-cell transport model for Potexviruses. Mol. Plant Microbe Interact. 18, 283-290.
76. Waadt, R., Schmidt, L. K., Lohse, M., Hashimoto, K., Bock, R., and Kudla, J. (2008). Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505-516.
77. Wei, T., Huang, T. S., McNeil, J., Laliberté, J. F., Hong, J., Nelson, R. S., et al. (2010). Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J. Virol. 84, 799-809.
78. Wu, C. H., Lee, S. C., and Wang, C. W. (2011). Viral protein targeting to the cortical endoplasmic reticulum is required for cell-cell spreading in plants. J. Cell Biol. 193, 521-535.
79. Xiang, Y., Kakani, K., Reade, R., Hui, E., and Rochon, D. (2006). A 38-amino-acid sequence encompassing the arm domain of the cucumber necrosis virus coat protein functions as a chloroplast transit peptide in infected plants. J. Virol. 80, 7952-7964.
80. Yan, F., Lu, Y., Lin, L., Zheng, H., and Chen, J. (2012). The ability of PVX p25 to form RL structures in plant cells is necessary for its function in movement, but not for its suppression of RNA silencing. PLoS ONE 7:e43242. doi:10.1371/journal.pone.0043242
81. Yang, C., Guo, R., Jie, F., Nettleton, D., Peng, J., Carr, T., et al. (2007). Spatial analysis of Arabidopsis thaliana gene expression in response to Turnip mosaic virus infection. Mol. Plant Microbe Interact. 20, 358-370.
82. Zhang, C., Liu, Y., Sun, X., Qian, W., Zhang, D., and Qiu, B. (2008). Characterization of a specific interaction between IP-L, a tobacco protein localized in thylakoid membranes, and Tomato mosaic virus coat protein. Biochem. Biophys. Res. Commun. 374, 253-257.