Identification of host proteins modulated by the virulence factor AC2 of Tomato chlorotic mottle virus in Nicotiana benthamiana

Proteomics

Volumn 13, Issue 12-13, 2013, Pages 1947-1960

  Carmo, Lilian Silveira Travassos ^a,b   Resende, Renato Oliveira ^b   Silva, Luciano Paulino ^a   Ribeiro, Simone Graça ^a   Mehta, Angela ^a  

^a EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^b UNIVERSITY OF BRASILIA   (Brazil)

Author keywords

Differential expression; Plant proteomics; Plant virus interaction; ToCMoV

Indexed keywords

ANNEXIN; CHAPERONIN; EPOXIDE HYDROLASE; GLUCAN ENDO 1,3 BETA GLUCOSIDASE; MALATE DEHYDROGENASE; MATURASE K; OXIDOREDUCTASE; PHOSPHOMANNOMUTASE; PROTEIN; PROTEIN DISULFIDE ISOMERASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SUCCINATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; VIRULENCE FACTOR AC2; VOLTAGE DEPENDENT ANION CHANNEL;

ARTICLE; CHLOROPLAST; CONTROLLED STUDY; DOWN REGULATION; ENERGY YIELD; GLYCOSYLATION; MAIZE CHLOROTIC MOTTLE; NICOTIANA BENTHAMIANA; OXIDATIVE STRESS; PHOTOSYNTHESIS; PLANT DEFENSE; PLANT DEVELOPMENT; PLANT DISEASE; PLASMODESMA; POTEXVIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RHIZOBIUM RADIOBACTER; TOMATO;

DIFFERENTIAL EXPRESSION; PLANT PROTEOMICS; PLANT-VIRUS INTERACTION; TOCMOV;

AGROBACTERIUM TUMEFACIENS; BASE SEQUENCE; BEGOMOVIRUS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, PLANT; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; POTEXVIRUS; PROTEOME; PROTEOMICS; SEQUENCE ALIGNMENT; TOBACCO; VIRAL PROTEINS; VIRULENCE FACTORS;

EID: 84880104029     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201200547     Document Type: Article

References (85)

1. Varma, A., Malathi, V. G., Emerging geminivirus problems: a serious threat to crop production. Ann. Appl. Biol. 2003, 142, 145-164.
2. Faria, J. C., Bezerra, I. C., Zerbini, F. M., Ribeiro, S. G., Lima, M. F., Situação atual das geminiviroses no Brasil. Fitopatol Bras 2000, 25, 125-137.
3. Albuquerque, L. C., Varsani, A., Fernandes, F. R., Pinheiro, B. et al., Further characterization of tomato-infecting begomoviruses in Brazil. Arch. Virol. 2012, 157, 747-752.
4. Castillo-Urquiza, G. P., Beserra, J. E., Jr., Bruckner, F. P., Lima, A. T. et al., Six novel begomoviruses infecting tomato and associated weeds in Southeastern Brazil. Arch. Virol. 2008, 153, 1985-1989.
5. Wang, H., Hao, L., Shung, C. Y., Sunter, G., Bisaro, D. M., Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 2003, 15, 3020-3032.
6. Yang, X., Baliji, S., Buchmann, R. C., Wang, H. et al., Functional modulation of the geminivirus AL2 transcription factor and silencing suppressor by self-interaction. J. Virol. 2007, 81, 11972-11981.
7. Sunter, G., Bisaro, D. M., Transactivation in a geminivirus: AL2 gene product is needed for coat protein expression. Virology 1991, 180, 416-419.
8. Sunter, G., Bisaro, D. M., Transactivation of geminivirus AR1 and BR1 gene expression by the viral AL2 gene product occurs at the level of transcription. Plant Cell 1992, 4, 1321-1331.
9. Trinks, D., Rajeswaran, R., Shivaprasad, P. V., Akbergenov, R. et al., Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J. Virol. 2005, 79, 2517-2527.
10. Baliji, S., Lacatus, G., Sunter, G., The interaction between geminivirus pathogenicity proteins and adenosine kinase leads to increased expression of primary cytokinin-responsive genes. Virology 2010, 402, 238-247.
11. Hao, L., Wang, H., Sunter, G., Bisaro, D. M., Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 2003, 15, 1034-1048.
12. Lozano-Duran, R., Bejarano, E. R., Geminivirus C2 protein might be the key player for geminiviral co-option of SCF-mediated ubiquitination. Plant Signal. Behav. 2011, 6, 999-1001.
13. Raja, P., Sanville, B. C., Buchmann, R. C., Bisaro, D. M., Viral genome methylation as an epigenetic defense against geminiviruses. J. Virol. 2008, 82, 8997-9007.
14. Sunter, G., Sunter, J. L., Bisaro, D. M., Plants expressing tomato golden mosaic virus AL2 or beet curly top virus L2 transgenes show enhanced susceptibility to infection by DNA and RNA viruses. Virology 2001, 285, 59-70.
15. Chapman, S., Kavanagh, T., Baulcombe, D., Potato virus X as a vector for gene expression in plants. Plant J. 1992, 2, 549-557.
16. Lacorte, C., Ribeiro, S. G., Lohuis, D., Goldbach, R., Prins, M., Potatovirus X and Tobacco mosaic virus-based vectors compatible with the Gateway cloning system. J. Virol. Methods 2010, 164, 7-13.
17. Amin, I., Patil, B. L., Briddon, R. W., Mansoor, S., Fauquet, C. M., Comparison of phenotypes produced in response to transient expression of genes encoded by four distinct begomoviruses in Nicotiana benthamiana and their correlation with the levels of developmental miRNAs. Virol. J. 2011, 8.
18. Hong, Y., Saunders, K., Stanley, J., Transactivation of dianthin transgene expression by African cassava mosaic virus AC2. Virology 1997, 228, 383-387.
19. Luna, A. P., Morilla, G., Voinnet, O., Bejarano, E. R., Functional analysis of gene-silencing suppressors from tomato yellow leaf curl disease viruses. Mol. Plant Microbe Interact. 2012, 25, 1294-1306.
20. Goodin, M. M., Zaitlin, D., Naidu, R. A., Lommel, S. A., Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol. Plant Microbe Interact. 2008, 21, 1015-1026.
21. Senthil-Kumar, S., Mysore, K. S., New dimensions for VIGS in plant functional genomics. Trends Plant Sci. 2011, 16, 656-665.
22. Voinnet, O., Rivas, S., Mestre, P., Baulcombe, D., An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 2003, 33, 949-956.
23. Ribeiro, S. G., Diversity and Host Interactions of Emerging Tomato Begomoviruses in Brazil, Starprint Gráfica e Editora, Brasília 2006.
24. Ribeiro, S. G., Martin, D. P., Lacorte, C., Simões, I. C. et al., Molecular and biological characterization of Tomato chlorotic mottle virus suggests that recombination underlies the evolution and diversity of Brazilian tomato begomoviruses. Phytopathology 2007, 97, 702-711.
25. Bucher, E., Hemmes, H., de Haan, P., Goldbach, R., Prins, M., The influenza A virus NS1 protein binds small interfering RNAs and suppresses RNA silencing in plants. J. Gen. Virol. 2004, 85, 983-991.
26. Mot, R. D., Vanderleyden, J., Application of two-dimensional protein analysis for strain fingerprinting and mutant analysis of Azospirillum species. Can. J. Microbiol. 1989, 35, 960-967.
27. Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68, 850-858.
28. Vanitharani, R., Chellappan, P., Pita, J. S., Fauquet, C. M., Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J. Virol. 2004, 78, 9487-9498.
29. Selth, L. A., Randles, J. W., Rezaian, M. A., Host responses to transient expression of individual genes encoded by Tomato leaf curl virus. Mol. Plant Microbe Interact. 2004, 17, 27-33.
30. Wang, H., Buckley, K. J., Yang, X. J., Buchmann, R. C., Bisaro, D. M., Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 2005, 79, 7410-7418.
31. Voinnet, O., Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 2005, 6, 206-220.
32. Rawat, N., Himabindu, K., Neeraja, C. N., Nair, S., Bentur, J. S., Suppressive subtraction hybridization reveals that rice gall midge attack elicits plant-pathogen-like responses in rice. Plant Physiol. Biochem. 2012, 63, 122-130.
33. Guimarães, P. M., Brasileiro, A. C., Morgante, C. V., Martins, A. C. et al., Global transcriptome analysis of two wild relatives of peanut under drought and fungi infection. BMC Genomics 2012, 13, 387.
34. Howard, A. R., Heppler, M. L., Ju, H. J., Krishnamurthy, K. et al., Potato virus X TGBp1 induces plasmodesmata gating and moves between cells in several host species whereas CP moves only in N. benthamiana leaves. Virology 2004, 328, 185-197.
35. Krishnamurthy, K., Mitra, R., Payton, M. E., Verchot-Lubicz, J., Cell-to-cell movement of the PVX 12K, 8K, or coat proteins may depend on the host, leaf developmental stage, and the PVX 25K protein. Virology 2002, 300, 269-281.
36. Voinnet, O., Lederer, C., Baulcombe, D. C., A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 2000, 103, 157-167.
37. Verchot-Lubicz, J., A new cell-to-cell transport model for Potexviruses. Mol. Plant Microbe Interact. 2005, 18, 283-290.
38. Atabekov, J. G., Rodionova, N. P., Karpova, O. V., Kozlovsky, S. V. et al., Translational activation of encapsidated potato virus X RNA by coat protein phosphorylation. Virology 2001, 286, 466-474.
39. Karpova, O. V., Arkhipenko, M. V., Zaiakina, O. V., Nikitin, N. A. et al., [Translational regulation of potato virus X RNA-coat protein complexes: the key role of a coat protein N-terminal peptide]. Mol. Biol. (Mosk) 2006, 40, 703-710.
40. Koenig, R., Anomalous behavior of the coat proteins of potato virus X and cactus virus X during electrophoresis in dodecyl sulfate-containing polyacrylamide gels. Virology 1972, 50, 263-266.
41. Bilgin, D. D., Zavala, J. A., Zhu, J., Clough, S. J. et al., Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ. 2010, 33, 1597-1613.
42. Hariharan, T., Johnson, P. J., Cattolico, R. A., Purification and characterization of phosphoribulokinase from the marine chromophytic alga Heterosigma carterae. Plant Physiol. 1998, 117, 321-329.
43. Chen, X., Yu, T., Xiong, J., Zhang, Y. et al., Molecular cloning and expression analysis of rice phosphoribulokinase gene that is regulated by environmental stresses. Mol. Biol. Rep. 2004, 31, 249-255.
44. Soitamo, A. J., Jada, B., Lehto, K., Expression of geminiviral AC2 RNA silencing suppressor changes sugar and jasmonate responsive gene expression in transgenic tobacco plants. BMC Plant Biol. 2012, 12, 204.
45. Soitamo, A. J., Jada, B., Lehto, K., HC-Pro silencing suppressor significantly alters the gene expression profile in tobacco leaves and flowers. BMC Plant. Biol. 2011, 11, 68.
46. Hennig, J., Herrmann, R., Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol. Gen. Genet. 1986, 203, 117-128.
47. Adi, M., Jens, P., Brotman, Y., Mikhail, K. et al., Stress responses to Tomato Yellow Leaf Curl Virus (TYLCV) infection of resistant and susceptible tomato plants are different. Metabolomics 2012, S1, 006.
48. Chivasa, S., Tomé, D. F., Hamilton, J. M., Slabas, A. R., Proteomic analysis of extracellular ATP-regulated proteins identifies ATP synthase beta-subunit as a novel plant cell death regulator. Mol. Cell Proteomics 2011, 10, M110.003905.
49. Chivasa, S., Ndimba, B. K., Simon, W. J., Lindsey, K., Slabas, A. R., Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 2005, 17, 3019-3034.
50. Andleeb, S., Amin, I., Bashir, A., Briddon, R. W., Mansoor, S., Transient expression of βC1 protein differentially regulates host genes related to stress response, chloroplast and mitochondrial functions. Virol. J. 2010, 7, 373.
51. David, P., des Francs-Small, C. C., Sévignac, M., Thareau, V. et al., Three highly similar formate dehydrogenase genes located in the vicinity of the B4 resistance gene cluster are differentially expressed under biotic and abiotic stresses in Phaseolus vulgaris. Theor. Appl. Genet. 2010, 121, 87-103.
52. Kusano, T., Tateda, C., Berberich, T., Takahashi, Y., Voltage-dependent anion channels: their roles in plant defense and cell death. Plant Cell Rep. 2009, 28, 1301-1308.
53. Glaser, E., Sjöling, S., Tanudji, M., Whelan, J., Mitochondrial protein import in plants. Signals, sorting, targeting, processing and regulation. Plant Mol. Biol. 1998, 38, 311-338.
54. Satoh, K., Kondoh, H., Sasaya, T., Shimizu, T. et al., Selective modification of rice (Oryza sativa) gene expression by rice stripe virus infection. J. Gen. Virol. 2010, 91, 294-305.
55. Beffa, R. S., Hofer, R. M., Thomas, M., Meins, F., Decreased susceptibility to viral disease of [beta]-1, 3-glucanase-deficient plants generated by antisense transformation. Plant Cell 1996, 8, 1001-1011.
56. Babu, M., Gagarinova, A. G., Brandle, J. E., Wang, A., Association of the transcriptional response of soybean plants with soybean mosaic virus systemic infection. J. Gen. Virol. 2008, 89, 1069-1080.
57. Verma, D. P., Hong, Z., Plant callose synthase complexes. Plant Mol. Biol. 2001, 47, 693-701.
58. Herbers, K., Tacke, E., Hazirezaei, M., Krause, K.-P. et al., Expression of a luteoviral movement protein in transgenic plants leads to carbohydrate accumulation and reduced photosynthetic capacity in source leaves. Plant J. 1997, 12, 1045-1056.
59. van Loon, L. C., Rep, M., Pieterse, C. M., Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 2006, 44, 135-162.
60. McKenzie, C. L., Shatters, R. G., Doostdar, H., Lee, S. D. et al., Effect of geminivirus infection and Bemisia infestation on accumulation of pathogenesis-related proteins in tomato. Arch. Insect. Biochem. Physiol. 2002, 49, 203-214.
61. Meldau, S., Baldwin, I. T., Wu, J., For security and stability: SGT1 in plant defense and development. Plant Signal. Behav. 2011, 6, 1479-1482.
62. Zhang, M., Botër, M., Li, K., Kadota, Y. et al., Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes. EMBO J. 2008, 27, 2789-2798.
63. Ye, C. M., Kelly, V., Payton, M., Dickman, M. B., Verchot, J., SGT1 is induced by the potato virus X TGBp3 and enhances virus accumulation in Nicotiana benthamiana. Mol. Plant 2012, 5, 1151-1153.
64. Lozano-Durán, R., Rosas-Díaz, T., Luna, A. P., Bejarano, E. R., Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS One 2011, 6, e22383.
65. Newman, J. W., Morisseau, C., Hammock, B. D., Epoxide hydrolases: their roles and interactions with lipid metabolism. Prog. Lipid. Res. 2005, 44, 1-51.
66. Zhou, L., Duan, J., Wang, X. M., Zhang, H. M. et al., Characterization of a novel annexin gene from cotton (Gossypium hirsutum cv CRI 35) and antioxidative role of its recombinant protein. J. Integr. Plant Biol. 2011, 53, 347-357.
67. Tunc-Ozdemir, M., Miller, G., Song, L., Kim, J. et al., Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol. 2009, 151, 421-432.
68. Andrawis, A., Solomon, M., Delmer, D. P., Cotton fiber annexins: a potential role in the regulation of callose synthase. Plant J. 1993, 3, 763-772.
69. Konopka-Postupolska, D., Clark, G., Hofmann, A., Structure, function and membrane interactions of plant annexins: an update. Plant Sci. 2011, 181, 230-241.
70. Levine, A. J., Hu, W., Feng, Z., The P53 pathway: what questions remain to be explored? Cell Death Differ. 2006, 13, 1027-1036.
71. Yao, Y. X., Dong, Q. L., Zhai, H., You, C. X., Hao, Y. J., The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses. Plant Physiol. Biochem. 2011, 49, 257-264.
72. Barthet, M. M., Hilu, K. W., Expression of matK: functional and evolutionary implications. Am. J. Bot. 2007, 94, 1402-1412.
73. Garavaglia, B. S., Thomas, L., Zimaro, T., Gottig, N. et al., A plant natriuretic peptide-like molecule of the pathogen Xanthomonas axonopodis pv. citri causes rapid changes in the proteome of its citrus host. BMC Plant Biol. 2010, 10, 51.
74. Zheng, X. M., Moncollin, V., Egly, J. M., Chambon, P., A general transcription factor forms a stable complex with RNA polymerase B (II). Cell 1987, 50, 361-368.
75. Brockstedt, E., Otto, A., Rickers, A., Bommert, K., Wittmann-Liebold, B., Preparative high-resolution two-dimensional electrophoresis enables the identification of RNA polymerase B transcription factor 3 as an apoptosis-associated protein in the human BL60-2 Burkitt lymphoma cell line. J. Protein Chem. 1999, 18, 225-231.
76. Yang, K. S., Kim, H. S., Jin, U. H., Lee, S. S. et al., Silencing of NbBTF3 results in developmental defects and disturbed gene expression in chloroplasts and mitochondria of higher plants. Planta 2007, 225, 1459-1469.
77. Huh, S. U., Kim, K. J., Paek, K. H., Capsicum annuum basic transcription factor 3 (CaBtf3) regulates transcription of pathogenesis-related genes during hypersensitive response upon tobacco mosaic virus infection. Biochem. Biophys. Res. Commun. 2012, 417, 910-917.
78. Ye, C., Dickman, M. B., Whitham, S. A., Payton, M., Verchot, J., The unfolded protein response is triggered by a plant viral movement protein. Plant Physiol. 2011, 156, 741-755.
79. Lu, D. P., Christopher, D. A., 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 2008, 280, 199-210.
80. Pedrazzini, E., Giovinazzo, G., Bollini, R., Ceriotti, A., Vitale, A., Binding of BiP to an assembly-defective protein in plant cells. Plant J. 1994, 5, 103-110.
81. Lee, A. S., The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 2001, 26, 504-510.
82. Krenz, B., Windeisen, V., Wege, C., Jeske, H., Kleinow, T., A plastid-targeted heat shock cognate 70 kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 2010, 401, 6-17.
83. Noël, L. D., Cagna, G., Stuttmann, J., Wirthmüller, L. et al., Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates arabidopsis immune responses. Plant Cell Online 2007, 19, 4061-4076.
84. Komatsu, K., Hashimoto, M., Ozeki, J., Yamaji, Y. et al., Viral induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol. Plant Microbe Interact. 2010, 23, 283-293.
85. Ahn, I. P., Kim, S., Lee, Y. H., Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol. 2005, 138, 1505-1515.