A protein kinase binds the C-terminal domain of the readthrough protein of Turnip yellows virus and regulates virus accumulation

Virology

Volumn 486, Issue , 2015, Pages 44-53

  Rodriguez Medina, Caren ^a,d   Boissinot, Sylvaine ^a   Chapuis, Sophie ^b   Gereige, Dalya ^a,e   Rastegar, Maryam ^a,f   Erdinger, Monique ^a   Revers, Frédéric ^c   Ziegler Graff, Véronique ^b   Brault, Véronique ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d CENTRO DE INVESTIGACIÓN TIBAITATÁ   (Colombia)

^e LEBANESE UNIVERSITY   (Lebanon)

^f SHIRAZ UNIVERSITY   (Iran)

Author keywords

CIPK; Kinase; Movement; Phloem; Plant; Polerovirus

Indexed keywords

CALCINEURIN; CALCINEURIN B LIKE PROTEIN INTERACTING PROTEIN KINASE 7; COMPLEMENTARY DNA; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CIPK7 PROTEIN, ARABIDOPSIS; PROTEIN BINDING; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; VIRUS PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA LIBRARY; DNA SYNTHESIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE CONSTRUCT; HOMOZYGOSITY; IMMUNOPRECIPITATION; INDEL MUTATION; MASS SPECTROMETRY; NICOTIANA BENTHAMIANA; NONHUMAN; PHLOEM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTOPLAST; REAL TIME POLYMERASE CHAIN REACTION; TURNIP YELLOW MOSAIC VIRUS; TWO HYBRID SYSTEM; VIRION; VIRUS TRANSCRIPTION; WESTERN BLOTTING; ARABIDOPSIS; CHEMISTRY; ENZYMOLOGY; GENETICS; HOST PATHOGEN INTERACTION; LUTEOVIRIDAE; METABOLISM; PLANT DISEASE; VIROLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; HOST-PATHOGEN INTERACTIONS; LUTEOVIRIDAE; PLANT DISEASES; PROTEIN BINDING; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; VIRAL PROTEINS;

EID: 84942097398     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.08.031     Document Type: Article

References (53)

1. 2+-regulated kinases. EMBO J. 2001, 20:1051-1063.
2. Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R., Gadrinab C., Heller C., Jeske A., Koesema E., Meyers C.C., Parker H., Prednis L., Ansari Y., Choy N., Deen H., Geralt M., Hazari N., Hom E., Karnes M., Mulholland C., Ndubaku R., Schmidt I., Guzman P., Aguilar-Henonin L., Schmid M., Weigel D., Carter D.E., Marchand T., Risseeuw E., Brogden D., Zeko A., Crosby W.L., Berry C.C., Ecker J.R. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301:653-657.
3. Amari K., Boutant E., Hofmann C., Schmitt-Keichinger C., Fernandez-Calvino L., Didier P., Lerich A., Mutterer J., Thomas C.L., Heinlein M., Mely Y., Maule A.J., Ritzenthaler C. A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog. 2010, 6:e1001119.
4. Batistic O., Kudla J. Analysis of calcium signaling pathways in plants. Biochim. Biophys. Acta 2012, 1820:1283-1293.
5. Baumberger N., Tsai C.H., Lie M., Havecker E., Baulcombe D.C. The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 2007, 17:1609-1614.
6. Beebe D.U., Russin W.A. Plasmodesmata in the phloem-loading pathway. Plasmodesmata: Structure, Function, Role in Cell Communication 1999, 261-293. Springer-Verlag, New-York. A.J.E. Van Bel, W.J.P. van Kesteren (Eds.).
7. 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 efficient systemic infection of plants. PloS ONE 2014, 9:e93448.
8. Bortolamiol D., Pazhouhandeh M., Marrocco K., Genschik P., Ziegler-Graff V. The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 2007, 17:1615-1621.
9. Brault V., Perigon S., Reinbold C., Erdinger M., Scheidecker D., Herrbach E., Richards K., Ziegler-Graff V. The Polerovirus minor capsid protein determines vector specificity and intestinal tropism in the aphid. J. Virol. 2005, 79:9685-9693.
10. Brault V., van den Heuvel J.F., Verbeek M., Ziegler-Graff V., Reutenauer A., Herrbach E., Garaud J.C., Guilley H., Richards K., Jonard G. Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74. EMBO J. 1995, 14:650-659.
11. Bruyère A., Brault V., Ziegler-Graff V., Simonis M.T., Van den Heuvel J.F., Richards K., Guilley H., Jonard G., Herrbach E. 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.
12. Chapuis S., Monsion B., Halter D., Rodriguez-Medina C., Baldenweck R., Thébaud G., Hugueney P., Revers F., Brault V. and Ziegler-Graff V. Profiling of phloem specific gene expression upon polerovirus infection, manuscript in preparation.
13. 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.
14. Clark M.F., Adams A.N. Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J. Gen. Virol. 1977, 34:475-483.
15. Csorba T., Lozsa R., Hutvagner G., Burgyan J. Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. Plant J 2010, 62:463-472.
16. Czechowski T., Stitt M., Altmann T., Udvardi M.K., Scheible W.R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005, 139:5-17.
17. D'Angelo C., Weinl S., Batistic O., Pandey G.K., Cheong Y.H., Schultke S., Albrecht V., Ehlert B., Schulz B., Harter K., Luan S., Bock R., Kudla J. Alternative complex formation of the Ca-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J. 2006, 48:857-872.
18. English J.J., Davenport G.F., Elmayan T., Vaucheret H., Baulcombe D.C. Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J. 1997, 12:597-603.
19. Gildow F. Luteovirus transmission mechanisms regulating vector specificity. The Luteoviridae 1999, 88-111. CAB International, Oxon, UK. H.G. Smith, H. Barker (Eds.).
20. Gong D., Guo Y., Jagendorf A.T., Zhu J.K. Biochemical characterization of the Arabidopsis protein kinase SOS2 that functions in salt tolerance. Plant Physiol. 2002, 130:256-264.
21. Guo Y., Halfter U., Ishitani M., Zhu J.K. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 2001, 13:1383-1400.
22. Halfter U., Ishitani M., Zhu J.K. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:3735-3740.
23. Holsters M., Silva B., Van Vliet F., Genetello C., De Block M., Dhaese P., Depicker A., Inze D., Engler G., Villarroel R., et al. The functional organization of the nopaline A. tumefaciens plasmid pTiC58. Plasmid 1980, 3:212-230.
24. Hruz T., Laule O., Szabo G., Wessendorp F., Bleuler S., Oertle L., Widmayer P., Gruissem W., Zimmermann P. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinform. 2008, 2008:420747.
25. Imlau A., Truernit E., Sauer N. Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 1999, 11:309-322.
26. Kang H.K., Yang S.H., Lee Y.P., Park Y.I., Kim S.H. A tobacco CBL-interacting protein kinase homolog is involved in phosphorylation of the N-terminal domain of the cucumber mosaic virus polymerase 2a protein. Biosci. Biotechnol. Biochem. 2012, 76:2101-2106.
27. Karimi M., Inze D., Depicker A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002, 7:193-195.
28. Kim S.H., Palukaitis P., Park Y.I. Phosphorylation of cucumber mosaic virus RNA polymerase 2a protein inhibits formation of replicase complex. EMBO J. 2002, 21:2292-2300.
29. Klein E., Brault V., Klein D., Weyens G., Lefebvre M., Ziegler-Graff V., Gilmer D. Divergence of host range and biological properties between natural isolate and full-length infectious cDNA clone of the Beet mild yellowing virus 2ITB. Mol. Plant Pathol. 2014, 15:22-30.
30. Kolukisaoglu U., Weinl S., Blazevic D., Batistic O., Kudla J. Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol. 2004, 134:43-58.
31. Kudla J., Xu Q., Harter K., Gruissem W., Luan S. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:4718-4723.
32. 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.
33. Leiser R.M., Ziegler-Graff V., Reutenauer A., Herrbach E., Lemaire O., Guilley H., Richards K., Jonard G. Agroinfection as an alternative to insects for infecting plants with beet western yellows luteovirus. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:9136-9140.
34. Liu J., Ishitani M., Halfter U., Kim C.S., Zhu J.K. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:3730-3734.
35. Mutterer J.D., Stussi-Garaud C., Michler P., Richards K.E., Jonard G., Ziegler-Graff V. Role of the beet western yellows virus readthrough protein in virus movement in Nicotiana clevelandii. J. Gen. Virol. 1999, 80:2771-2778.
36. Ohta M., Guo Y., Halfter U., Zhu J.K. A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11771-11776.
37. Oparka K.J., Cruz S.S. THE GREAT ESCAPE: phloem transport and unloading of macromolecules1. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000, 51:323-347.
38. Pazhouhandeh M., Dieterle M., Marrocco K., Lechner E., Berry B., Brault V., Hemmer O., Kretsch T., Richards K.E., Genschik P., Ziegler-Graff V. F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1994-1999.
39. 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.
40. 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.
41. Quan R., Lin H., Mendoza I., Zhang Y., Cao W., Yang Y., Shang M., Chen S., Pardo J.M., Guo Y. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 2007, 19:1415-1431.
42. Reinbold C., Lacombe S., Ziegler-Graff V., Scheidecker D., Wiss L., Beuve M., Caranta C., Brault V. Closely related poleroviruses depend on distinct translation initiation factors to infect Arabidopsis thaliana. Mol. Plant Microbe Interact. 2013, 26:257-265.
43. Reutenauer A., Ziegler-Graff V., Lot H., Scheidecker D., Guilley H., Richards K., Jonard G. Identification of beet western yellows luteovirus genes implicated in viral replication and particle morphogenesis. Virology 1993, 195:692-699.
44. Revollon S., Strub J.M., Fitchette A.C., Wiss L., Gomord V., Van Dorsselaer A., Brault V. A reinvestigation provides no evidence for sugar residues on structural proteins of poleroviruses and argues against a role for glycosylation of virus structural proteins in aphid transmission. Virology 2010, 402:303-314.
45. Roberts A.G., Oparka K. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 2003, 26:103-124.
46. Schmitz J., Stussi-Garaud C., Tacke E., Prufer D., Rohde W., Rohfritsch O. In situ localization of the putative movement protein (pr17) from potato leafroll luteovirus (PLRV) in infected and transgenic potato plants. Virology 1997, 235:311-322.
47. + antiporter. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:6896-6901.
48. Sokolova M., Prufer D., Tacke E., Rohde W. The potato leafroll virus 17K movement protein is phosphorylated by a membrane-associated protein kinase from potato with biochemical features of protein kinase C. FEBS Lett. 1997, 400:201-205.
49. Tacke E., Prufer D., Schmitz J., Rohde W. The potato leafroll luteovirus 17K protein is a single-stranded nucleic acid-binding protein. J. Gen. Virol. 1991, 72:2035-2038.
50. Tacke E., Schmitz J., Prufer D., Rohde W. Mutational analysis of the nucleic acid-binding 17 kDa phosphoprotein of potato leafroll luteovirus identifies an amphipathic alpha-helix as the domain for protein/protein interactions. Virology 1993, 197:274-282.
51. 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.
52. Weinl S., Kudla J. The CBL-CIPK Ca(2+)-decoding signaling network: function and perspectives. New Phytol. 2009, 184:517-528.
53. Ziegler-Graff V., Brault V., Mutterer J., Simonis M.T., Herrbach E., Guilley H., Richards K., Jonard G. The coat protein of beet western yellows luteovirus is essential for systemic infection but the viral gene products P29 and P19 are dispensable for systemic infection and aphid transmission. Mol. Plant Microbe Interact. 1996, 9:501-510.