Potato leafroll virus structural proteins manipulate overlapping, yet distinct protein interaction networks during infection

Proteomics

Volumn 15, Issue 12, 2015, Pages 2098-2112

  Deblasio, Stacy L ^a,b   Johnson, Richard ^c   Sweeney, Michelle M ^a   Karasev, Alexander ^d   Gray, Stewart M ^b,e   Maccoss, Michael J ^c   Cilia, Michelle ^a,b,e  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF IDAHO   (United States)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

Affinity purification MS; Luteoviridae, Polerovirus; Plant proteomics; Potato leafroll virus; Readthrough protein

Indexed keywords

COAT PROTEIN; READTHROUGH PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; VIRUS PROTEIN;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; IMMUNOPRECIPITATION; MASS SPECTROMETRY; NICOTIANA BENTHAMIANA; NONHUMAN; PHLOEM; PLANT TISSUE; POTATO LEAFROLL VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; READ THROUGH DOMAIN; VIRAL PLANT DISEASE; VIRUS INFECTION; LUTEOVIRIDAE; METABOLISM; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; POTATO; PROCEDURES; PROTEIN PROTEIN INTERACTION; PROTEOMICS; VIROLOGY; WESTERN BLOTTING;

HEXAPODA; LUTEOVIRIDAE; POLEROVIRUS; POTATO LEAFROLL VIRUS;

BLOTTING, WESTERN; IMMUNOPRECIPITATION; LUTEOVIRIDAE; MASS SPECTROMETRY; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PROTEIN INTERACTION MAPS; PROTEOMICS; SOLANUM TUBEROSUM; VIRAL STRUCTURAL PROTEINS;

EID: 84931006440     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400594     Document Type: Article

References (114)

1. Gray, S. M., Cilia, M., Ghanim, M., in: Maramorosch, K., Murphy, F. A. (Eds.), Advances in Virus Research, Elsevier, San Diego, CA 2014, pp. 141-199.
2. Scholthof, K.-B. G., Scholthof, H. B., Jackson, A., The tomato bushy stunt virus replicase proteins are coordinately expressed and membrane associated. Virology 1995, 208, 365-369.
3. Beier, H., Barciszewska, M., Krupp, G., Mitnacht, R., Gross, H. J., UAG readthrough during TMV RNA translation: isolation and sequence of two tRNAsTyr with suppressor activity from tobacco plants. EMBO J. 1984, 3, 351.
4. Chay, C. A., Gunasinge, U. B., Dinesh-Kumar, S. P., Miller, W. A., Gray, S. M., Aphid transmission and systemic plant infection determinants of barley yellow dwarf luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively. Virology 1996, 219, 57-65.
5. Tamada, T., Schmitt, C., Saito, M., Guilley, H. et al., High resolution analysis of the readthrough domain of beet necrotic yellow vein virus readthrough protein: a KTER motif is important for efficient transmission of the virus by Polymyxa betae. J. Gen. Virol. 1996, 77, 1359-1367.
6. Bruyere, A., Brault, V., Ziegler-Graff, V., Simonis, M. T. et al., Effects of mutations in the beet western yellows virus readthrough protein on its expression and packaging and on virus accumulation, symptoms, and aphid transmission. Virology 1997, 230, 323-334.
7. Peter, K. A., Liang, D., Palukaitis, P., Gray, S. M., Small deletions in the Potato leafroll virus readthrough protein affect particle morphology, aphid transmission, virus movement and accumulation. J. Gen. Virol. 2008, 89, 2037-2045.
8. Peter, K. A., Gildow, F., Palukaitis, P., Gray, S. M., The C terminus of the polerovirus p5 readthrough domain limits virus infection to the phloem. J. Virol. 2009, 83, 5419-5429.
9. Cowan, G., Torrance, L., Reavy, B., Detection of potato mop-top virus capsid readthrough protein in virus particles. J. Gen. Virol. 1997, 78, 1779-1783.
10. Chavez, J. D., Cilia, M., Weisbrod, C. R., Ju, H. J. et al., Cross-linking measurements of the Potato leafroll virus reveal protein interaction topologies required for virion stability, aphid transmission, and virus-plant interactions. J. Proteome Res. 2012, 11, 2968-2981.
11. Boissinot, S., Erdinger, M., Monsion, B., Ziegler-Graff, V., Brault, V., Both structural and non-structural forms of the readthrough protein of Cucurbit aphid-borne yellows virus are essential for effficient systemic infection of plants. PloS One 2014, 9, e93448.
12. Dreher, T. W., Miller, W. A., Translational control in positive strand RNA plant viruses. Virology 2006, 344, 185-197.
13. Torrance, L., Analysis of epitopes on potato leafroll virus capsid protein. Virology 1992, 191, 485-489.
14. Filichkin, S. A., Lister, R. M., McGrath, P. F., Young, M. J., In vivo expression and mutational analysis of the barley yellow dwarf virus readthrough gene. Virology 1994, 205, 290-299.
15. Perry, K. L., Miller, J., Lister, R. M., Mayo, M. A., Luteovirus isolation and RNA extraction. Methods Mol. Biol. 1998, 81, 231-239.
16. Wang, J. Y., Chay, C., Gildow, F. E., Gray, S. M., Readthrough protein associated with virions of barley yellow dwarf luteovirus and its potential role in regulating the efficiency of aphid transmission. Virology 1995, 206, 954-962.
17. DeBlasio, S. L., Johnson, R., Mahoney, J., Karasev, A. et al., Insights into the polerovirus-plant interactome revealed by co-immunoprecipitation and mass spectrometry. Mol. Plant Microbe Interact. 2014, MPMI-11-14-0363-R.
18. Bencharki, B., Boissinot, S., Revollon, S., Ziegler-Graff, V. et al., Phloem protein partners of Cucurbit aphid borne yellows virus: possible involvement of phloem proteins in virus transmission by aphids. Mol. Plant. Microbe Interact. 2010, 23, 799-810.
19. Cilia, M., Peter, K. A., Bereman, M. S., Howe, K. et al., Discovery and targeted LC-MS/MS of purified polerovirus reveals differences in the virus-host interactome associated with altered aphid transmission. PLoS One 2012, 7, e48177.
20. Brault, V., Mutterer, J., Scheidecker, D., Simonis, M. T. et al., Effects of point mutations in the readthrough domain of the beet western yellows virus minor capsid protein on virus accumulation in planta and on transmission by aphids. J. Virol. 2000, 74, 1140-1148.
21. Liang, D., Gray, S. M., Kaplan, I., Palukaitis, P., Site-directed mutagenesis and generation of chimeric viruses by homologous recombination in yeast to facilitate analysis of plant-virus interactions. Mol. Plant Microbe Interact. 2004, 17, 571-576.
22. Lee, L., Kaplan, I. B., Ripoll, D. R., Liang, D. et al., A surface loop of the potato leafroll virus coat protein is involved in virion assembly, systemic movement, and aphid transmission. J. Virol. 2005, 79, 1207-1214.
23. Reinbold, C., Gildow, F. E., Herrbach, E., Ziegler-Graff, V. et al., Studies on the role of the minor capsid protein in transport of Beet western yellows virus through Myzus persicae. J. Gen. Virol. 2001, 82, 1995-2007.
24. Davis, M. T., Spahr, C. S., McGinley, M. D., Robinson, J. H. et al., Towards defining the urinary proteome using liquid chromatography-tandem mass spectrometry. II. Limitations of complex mixture analyses. Proteomics 2001, 1, 108-117.
25. Spahr, C. S., Davis, M. T., McGinley, M. D., Robinson, J. H. et al., Towards defining the urinary proteome using liquid chromatography-tandem mass spectrometry. I. Profiling an unfractionated tryptic digest. Proteomics 2001, 1, 93-107.
26. Perkins, D. N., Pappin, D. J., Creasy, D. M., Cottrell, J. S., Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20, 3551-3567.
27. Koskinen, V. R., Emery, P. A., Creasy, D. M., Cottrell, J. S., Hierarchical clustering of shotgun proteomics data. Mol. Cell. Proteomics 2011, 10, 1-12.
28. Nesvizhskii, A. I., Keller, A., Kolker, E., Aebersold, R., A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75, 4646-4658.
29. Pinheiro, P., Bereman, M. S., Burd, J., Pals, M. et al., Evidence of the biochemical basis of host virulence in the greenbug aphid, Schizaphis graminum (Homoptera: Aphididae). J. Proteome Res. 2014, 13, 2094-2108.
30. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M. et al., Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 2010, 26, 966-968.
31. Mellacheruvu, D., Wright, Z., Couzens, A. L., Lambert, J. P. et al., The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat. Methods 2013, 10, 730-736.
32. Choi, H., Liu, G., Mellacheruvu, D., Tyers, M. et al., Analyzing protein-protein interactions from affinity purification-mass spectrometry data with SAINT. Curr. Protoc. Bioinformatics 2012, Chapter 8, Unit8 15.
33. Choi, H., Larsen, B., Lin, Z. Y., Breitkreutz, A. et al., SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat. Methods 2011, 8, 70-73.
34. Moon, S., Han, D., Kim, Y., Jin, J. et al., Interactome analysis of AMP-activated protein kinase (AMPK)-alpha1 and -beta1 in INS-1 pancreatic beta-cells by affinity purification-mass spectrometry. Sci. Rep. 2014, 4, 4376.
35. Skarra, D. V., Goudreault, M., Choi, H., Mullin, M. et al., Label-free quantitative proteomics and SAINT analysis enable interactome mapping for the human Ser/Thr protein phosphatase 5. Proteomics 2011, 11, 1508-1516.
36. Smith-Kinnaman, W. R., Berna, M. J., Hunter, G. O., True, J. D. et al., The interactome of the atypical phosphatase Rtr1 in Saccharomyces cerevisiae. Mol. Biosyst. 2014, 10, 1730-1741.
37. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S. et al., Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13, 2498-2504.
38. Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P. et al., ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 2009, 25, 1091-1093.
39. Hochberg, Y., Benjamini, Y., More powerful procedures for multiple significance testing. Stat. Med. 1990, 9, 811-818.
40. Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L., Ideker, T., Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27, 431-432.
41. Tanz, S. K., Castleden, I., Hooper, C. M., Vacher, M. et al., SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res. 2013, 41, D1185-D1191.
42. Cilia, M., Fish, T., Yang, X., McLaughlin, M. et al., A comparison of protein extraction methods suitable for gel-based proteomic studies of aphid proteins. J. Biomol. Tech. 2009, 20, 201-215.
43. Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G., ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 2012, 35, 259-270.
44. Torres, M. A., Jones, J. D., Dangl, J. L., Reactive oxygen species signaling in response to pathogens. Plant Physiol. 2006, 141, 373-378.
45. Bradley, D. J., Kjellbom, P., Lamb, C. J., Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 1992, 70, 21-30.
46. Guilley, H., Wipf-Scheibel, C., Richards, K., Lecoq, H., Jonard, G., Nucleotide sequence of cucurbit aphid-borne yellows luteovirus. Virology 1994, 202, 1012-1017.
47. Hipper, C., Monsion, B., Bortolamiol-Bécet, D., Ziegler-Graff, V., Brault, V., Formation of virions is strictly required for turnip yellows virus long-distance movement in plants. J. Gen. Virol. 2014, 95, 496-505.
48. Lee, L., Palukaitis, P., Gray, S. M., Host-dependent requirement for the Potato leafroll virus 17-kda protein in virus movement. Mol. Plant Microbe Interact. 2002, 15, 1086-1094.
49. Marks, C. E., Newbigin, E., Ladiges, P. Y., Comparative morphology and phylogeny of Nicotiana section Suaveolentes (Solanaceae) in Australia and the South Pacific. Aust. Syst. Bot. 2011, 24, 61-86.
50. Mutterer, J. D., Stussi-Garaud, C., Michler, P., Richards, K. E. et al., Role of the beet western yellows virus readthrough protein in virus movement in Nicotiana clevelandii. J. Gen. Virol. 1999, 80, 2771-2778.
51. Hooks, M. A., Allwood, J. W., Harrison, J. K., Kopka, J. et al., Selective induction and subcellular distribution of ACONITASE 3 reveal the importance of cytosolic citrate metabolism during lipid mobilization in Arabidopsis. Biochem. J. 2014, 463, 309-317.
52. Gupta, K. J., Shah, J. K., Brotman, Y., Jahnke, K. et al., Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J. Exp. Bot. 2012, 63, 1773-1784.
53. Klessig, D. F., Durner, J., Noad, R., Navarre, D. A. et al., Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. USA 2000, 97, 8849-8855.
54. Whitham, S. A., Yang, C., Goodin, M. M., Global impact: elucidating plant responses to viral infection. Mol. Plant Microbe Interact. 2006, 19, 1207-1215.
55. Xu, X. M., Wang, J., Xuan, Z., Goldshmidt, A. et al., Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 2011, 333, 1141-1144.
56. Fichtenbauer, D., Xu, X. M., Jackson, D., Kragler, F., The chaperonin CCT8 facilitates spread of tobamovirus infection. Plant Signal Behav. 2012, 7, 318-321.
57. Zhang, Z., Quick, M. K., Kanelakis, K. C., Gijzen, M., Krishna, P., Characterization of a plant homolog of hop, a cochaperone of hsp90. Plant Physiol. 2003, 131, 525-535.
58. Postaire, O., Tournaire-Roux, C., Grondin, A., Boursiac, Y. et al., A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol. 2010, 152, 1418-1430.
59. Preger, V., Tango, N., Marchand, C., Lemaire, S. D. et al., Auxin-responsive genes AIR12 code for a new family of plasma membrane b-type cytochromes specific to flowering plants. Plant Physiol. 2009, 150, 606-620.
60. Velasquez, A. C., Chakravarthy, S., Martin, G. B., Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. J. Vis. Exp. 2009, 28, 1292.
61. Di Carli, M., Benvenuto, E., Donini, M., Recent insights into plant-virus interactions through proteomic analysis. J. Proteome Res. 2012, 11, 4765-4780.
62. Sampol, B., Bota, J., Riera, D., Medrano, H., Flexas, J., Analysis of the virus-induced inhibition of photosynthesis in malmsey grapevines. N. Phytol. 2003, 160, 403-412.
63. Tu, C. J., Ford, R. E., Kraus, C. J., Comparison of chloroplast and photosynthetic rates of plants infected and not infected by maize dwarf virus. Phytopathology 1967, 58, 285-288.
64. Zaitlin, M., Hull, R., Plant virus-host interactions. Annu. Rev. Plant Physiol. 1987, 38, 291-315.
65. Hodgson, R. A., Beachy, R. N., Pakrasi, H. B., Selective inhibition of photosystem II in spinach by tobacco mosaic virus: an effect of the viral coat protein. FEBS Lett. 1989, 245, 267-270.
66. Rahoutei, J., García-Luque, I., Barón, M., Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol. Plant. 2000, 110, 286-292.
67. Reinero, A., Beachy, R. N., Reduced photosystem II activity and accumulation of viral coat protein in chloroplasts of leaves infected with Tobacco mosaic virus. Plant Physiol. 1989, 89, 111-116.
68. Takahashi, H., Ehara, Y., 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. 1992, 1, 243-249.
69. Banerjee, N., Wang, J. Y., Zaitlin, M., A single nucleotide change in the coat protein gene of tobacco mosaic is involved in the induction of severe chlorosis. Virology 1995, 207, 234-239.
70. Bosque-Perez, N. A., Eigenbrode, S. D., The influence of virus-induced changes in plants on aphid vectors: insights from luteovirus pathosystems. Virus Res. 2011, 159, 201-205.
71. Eigenbrode, S. D., Ding, H., Shiel, P., Berger, P. H., Volatiles from potato plants infected with Potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc. Biol. Sci. 2002, 269, 455-460.
72. Livingston, D. P., Gildow, F. E., Barley yellow dwarf virus effects fructan and sugar concentration in winter oat crowns. Crop Sci. 1991, 31, 1081-1082.
73. Holmes, J. C., Bethel, W. M., in: Canning, E. U., Wright, C. A. (Eds.), Behavioural Aspects of Parasite Transmission, Academic Press, London 1972, pp. 123-149.
74. Loizeau, K., Gambonnet, B., Zhang, G. F., Curien, G. et al., Regulation of one-carbon metabolism in Arabidopsis: the N-terminal regulatory domain of cystathionine gamma-synthase is cleaved in response to folate starvation. Plant Physiol. 2007, 145, 491-503.
75. Mélida, H., Caparrós-Ruiz, D., Álvarez, J., Acebes, J. L., Encina, A., Deepening into the proteome of maize cells habituated to the cellulose biosynthesis inhibitor dichlobenil. Plant Signal. Behav. 2011, 6, 143-146.
76. Kawalleck, P., Plesch, G., Hahlbrock, K., Somssich, I. E., Induction by fungal elicitor of S-adenosyl-L-methionine synthetase and S-adenosyl-L-homocysteine hydrolase mRNAs in cultured cells and leaves of Petroselinum crispum. Proc. Natl. Acad. Sci. USA 1992, 89, 1713-4717.
77. Oide, S., Bejai, S., Staal, J., Guan, N., Kaliff, M., Dixelius C., A novel role of PR2 in abscisic acid (ABA) mediated, pathogen-induced callose deposition in Arabidopsis thaliana. N. Phytol. 2013, 200, 1187-1199.
78. Karkonen, A., Murigneux, A., Martinant, J. P., Pepey, E. et al., UDP-glucose dehydrogenases of maize: a role in cell wall pentose biosynthesis. Biochem. J. 2005, 391, 409-415.
79. Sampedro, J., Pardo, B., Gianzo, C., Guitian, E. et al., Lack of alpha-xylosidase activity in Arabidopsis alters xyloglucan composition and results in growth defects. Plant Physiol. 2010, 154, 1105-1115.
80. Benitez-Alfonso, Y., Faulkner, C., Ritzenthaler, C., Maule, A. J., Plasmodesmata: gateways to local and systemic virus infection. Mol. Plant Microbe Interact. 2010, 23, 1403-1412.
81. Gildow, F. E., in: Harris, K. F. (Ed.), Current Topics in Vector Research, Springer-Verlag, New York 1987, pp. 93-120.
82. Gildow, F. E., Evidence for receptor-mediated endocytosis regulating luteovirus acquisition by aphids. Phytopathology 1993, 83, 270-277.
83. Gildow, F. E., Gray, S. M., The aphid salivary gland basal lamina as a selective barrier associated with vector specific transmission of barley yellow dwarf luteoviruses. Phytopathology 1993, 83, 1293-1302.
84. Golinowski, W., Tomenius, K., Oxelfelt, P., Ultrastructural studies on potato phloem cells infected with Potato leafroll virus-comparison of two potato varieties. Acta Agric. Scand. 1987, 37, 3-19.
85. Shepardson, S., Esau, K., McCrum, R., Ultrastructure of potato leaf phloem infected with Potato leafroll virus. Virology 1980, 105, 379-392.
86. Eckardt, N. A., An exocyst vesicle tethering complex in plants. Plant Cell 2008, 20, 1188.
87. Schumacher, K., Endomembrane proton pumps: connecting membrane and vesicle transport. Curr. Opin. Plant Biol. 2006, 9, 595-600.
88. Jin, H., Li, S., Villegas, A., Jr., Down-regulation of the 26S proteasome subunit RPN9 inhibits viral systemic transport and alters plant vascular development. Plant Physiol. 2006, 142, 651-661.
89. UniProt, C., Activities at the universal protein resource (UniProt). Nucleic Acids Res. 2014, 42, D191-D198.
90. Brizard, J. P., Carapito, C., Delalande, F., VanDorsselaer, A., Brugidou, C., Proteome analysis of plant-virus interactome: comprehensive data for virus multiplication inside their hosts. Mol. Cell. Proteomics 2006, 5, 2279-2297.
91. Mhamdi, A., Mauve, C., Gouia, H., Saindrenan, P. et al., Cytosolic NADP-dependent isocitrate dehydrogenase contributes to redox homeostasis and the regulation of pathogen responses in Arabidopsis leaves. Plant Cell Environ. 2010, 33, 1112-1123.
92. Xu, Q., Ni, H., Chen, Q., Sun, F. et al., Comparative proteomic analysis reveals the cross-talk between the responses induced by H2O2 and by long-term rice black-streaked dwarf virus infection in rice. PLoS One 2013, 8, e81640.
93. Pan, X., Zhu, B., Luo, Y., Fu, D., Unraveling the protein network of tomato fruit in response to necrotrophic phytopathogenic Rhizopus nigricans. PLoS One 2013, 8, e73034.
94. Pitzschke, A., Djamei, A., Bitton, F., Hirt, H., A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol. Plant 2009, 2, 120-137.
95. Chivasa, S., Tome, D. F., Slabas, A. R., UDP-glucose pyrophosphorylase is a novel plant cell death regulator. J. Proteome Res. 2013, 12, 1743-1753.
96. Huitema, E., Vleeshouwers, V. G., Francis, D. M., Kamoun, S., Active defence responses associated with non-host resistance of Arabidopsis thaliana to the oomycete pathogen Phytophthora infestans. Mol. Plant Pathol. 2003, 4, 487-500.
97. Hyodo, K., Mine, A., Taniguchi, T., Kaido, M. et al., ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus. J. Virol. 2013, 87, 163-176.
98. Vandeputte, O., Lowe, Y. O., Burssens, S., VAN Raemdonck, D. et al., The tobacco Ntann12 gene, encoding an annexin, is induced upon Rhodoccocus fascians infection and during leafy gall development. Mol. Plant Pathol. 2007, 8, 185-194.
99. Wei, T., Wang, A., Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J. Virol. 2008, 82, 12252-12264.
100. Pecenkova, T., Hala, M., Kulich, I., Kocourkova, D. et al., The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. J. Exp. Bot. 2011, 62, 2107-2116.
101. Peiro, A., Izquierdo-Garcia, A. C., Sanchez-Navarro, J. A., Pallas, V. et al., Patellins 3 and 6, two members of the Plant Patellin family, interact with the movement protein of Alfalfa mosaic virus and interfere with viral movement. Mol. Plant Pathol. 2014, 15, 881-891.
102. Jones, A. M., Thomas, V., Bennett, M. H., Mansfield, J., Grant, M., Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol. 2006, 142, 1603-1620.
103. Muller, K., Doubnerova, V., Synkova, H., Cerovska, N., Ryslava, H., Regulation of phosphoenolpyruvate carboxylase in PVY(NTN)-infected tobacco plants. Biol. Chem. 2009, 390, 245-251.
104. Ghimire, S. R., Baird, S. M., Baker, G. T., Ma, P. W. K., Analysis of proteins associated with Chinch bug (Blissus leucopterus leucopterus Say)-infested corn (Zea mays L.) seedlings. Open Proteomics J. 2009, 2, 20-29.
105. Niehl, A., Amari, K., Gereige, D., Brandner, K. et al., Control of Tobacco mosaic virus movement protein fate by CELL-DIVISION-CYCLE protein48. Plant Physiol. 2012, 160, 2093-2108.
106. Floerl, S., Majcherczyk, A., Possienke, M., Feussner, K. et al., Verticillium longisporum infection affects the leaf apoplastic proteome, metabolome, and cell wall properties in Arabidopsis thaliana. PLoS One 2012, 7, e31435.
107. Peroni, L. A., Ferreira, R. R., Figueira, A., Machado, M. A., Stach-Machado, D. R., Expression profile of oxidative and antioxidative stress enzymes based on ESTs approach of citrus. Genet. Mol. Biol. 2007, 30, 872-880.
108. Palma, K., Zhao, Q., Cheng, Y. T., Bi, D. et al., Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes Dev. 2007, 21, 1484-1493.
109. Monaghan, J., Li, X., The HEAT repeat protein ILITYHIA is required for plant immunity. Plant Cell Physiol. 2010, 51, 742-753.
110. Chivasa, S., Tomé, D. F. A., Hamilton, J. M., Slabas, S. A., Proteomic analysis of extracellular ATP-regulated proteins identifies ATP synthase β-subunit as a novel plant cell death regulator. Mol. Cell. Proteomics 2011, 10, M110.003905.
111. Oh, C. S., Pedley, K. F., Martin, G. B., Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK {alpha}. Plant Cell 2010, 22, 260-272.
112. Seddas, P., Boissinot, S., Strub, J. M., Van Dorsselaer, A. et al., Rack-1, GAPDH3, and actin: proteins of Myzus persicae potentially involved in the transcytosis of beet western yellows virus particles in the aphid. Virology 2004, 325, 399-412.
113. Takeshit, D., Tomita, K., Assembly of Q{beta} viral RNA polymerase with host translational elongation factors EF-Tu and -Ts. Proc. Natl. Acad. Sci. USA 2010, 107, 15733-15738.
114. Fu, Z. Q., Guo, M., Jeong, B. R., Tian, F. et al., A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 2007, 447, 284-288.