Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Vijayapalani, Paramasivan ^a   Maeshima, Masayoshi ^b   Nagasaki Takekuchi, Nahoko ^b   Miller, W Allen ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

P3N PIPO PROTEIN; PCAP1 PROTEIN; PLANT VIRUS MOVEMENT PROTEIN; PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; PCAP1 PROTEIN, ARABIDOPSIS; VIRUS RNA;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CELL MOTION; CONTROLLED STUDY; HYDROPHILICITY; MYRISTYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POTYVIRUS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA REPLICATION; RNA SYNTHESIS; VIRUS CELL INTERACTION; YEAST CELL; GENE SILENCING; GENETICS; METABOLISM; OPEN READING FRAME; PHYSIOLOGY; PLANT DISEASE; SACCHAROMYCES CEREVISIAE; TRANSGENIC PLANT; TWO HYBRID SYSTEM; VIROLOGY; VIRUS GENOME;

ARABIDOPSIS; CHINESE RAPE MOSAIC VIRUS; POTYVIRUS; TOBAMOVIRUS; TURNIP MOSAIC VIRUS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CELL MEMBRANE; GENE KNOCKDOWN TECHNIQUES; GENOME, VIRAL; OPEN READING FRAMES; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; POTYVIRUS; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL PROTEINS;

EID: 84861210660     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002639     Document Type: Article

References (49)

1. Lucas WJ, Ham BK, Kim JY, (2009) Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell Biol 19: 495-503.
2. Maule AJ, Benitez-Alfonso Y, Faulkner C, (2011) Plasmodesmata - membrane tunnels with attitude. Curr Opin Plant Biol 14: 683-690.
3. Boevink P, Oparka KJ, (2005) Virus-host interactions during movement processes. Plant Physiol 138: 1815-1821.
4. Ueki S, Citovsky V, (2011) To Gate, or Not to Gate: Regulatory Mechanisms for Intercellular Protein Transport and Virus Movement in Plants. Mol Plant 4: 782-793.
5. Verchot-Lubicz J, Torrance L, Solovyev AG, Morozov SY, Jackson AO, et al. (2010) Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 23: 1231-1247.
6. Niehl A, Heinlein M, (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248: 75-99.
7. Harries P, Ding B, (2011) Cellular factors in plant virus movement: at the leading edge of macromolecular trafficking in plants. Virology 411: 237-243.
8. Laporte C, Vetter G, Loudes AM, Robinson DG, Hillmer S, et al. (2003) Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15: 2058-2075.
9. Riechmann JL, Lain S, Garcia JA, (1992) Highlights and prospects of potyvirus molecular biology. J Gen Virol 73: 1-16.
10. Urcuqui-Inchima S, Haenni AL, Bernardi F, (2001) Potyvirus proteins: a wealth of functions. Virus Res 74: 157-175.
11. Chung BY-W, Miller WA, Atkins JF, Firth AE, (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci U S A 105: 5897-5902.
12. Shen W, Yan P, Gao L, Pan X, Wu J, et al. (2010) Helper component-proteinase (HC-Pro) protein of Papaya ringspot virus interacts with papaya calreticulin. Mol Plant Pathol 11: 335-346.
13. Dolja VV, Haldeman R, Robertson NL, Dougherty WG, Carrington JC, (1994) Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J 13: 1482-1491.
14. Dolja VV, Haldeman-Cahill R, Montgomery AE, Vandenbosch KA, Carrington JC, (1995) Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology 206: 1007-1016.
15. Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ, (1997) Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237: 283-295.
16. Hofius D, Maier AT, Dietrich C, Jungkunz I, Bornke F, et al. (2007) Capsid protein-mediated recruitment of host DnaJ-like proteins is required for Potato virus Y infection in tobacco plants. J Virol 81: 11870-11880.
17. Rodriguez-Cerezo E, Findlay K, Shaw JG, Lomonossoff GP, Qiu SG, et al. (1997) The coat and cylindrical inclusion proteins of a potyvirus are associated with connections between plant cells. Virology 236: 296-306.
18. Dunoyer P, Thomas C, Harrison S, Revers F, Maule A, (2004) A cysteine-rich plant protein potentiates Potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol 78: 2301-2309.
19. Carrington JC, Jensen PE, Schaad MC, (1998) Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant J 14: 393-400.
20. Roberts IM, Wang D, Findlay K, Maule AJ, (1998) Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (Cls) show that the Cl protein acts transiently in aiding virus movement. Virology 245: 173-181.
21. Choi IR, Horken KM, Stenger DC, French R, (2005) An internal RNA element in the P3 cistron of Wheat streak mosaic virus revealed by synonymous mutations that affect both movement and replication. J Gen Virol 86: 2605-2614.
22. Wen RH, Hajimorad MR, (2010) Mutational analysis of the putative pipo of soybean mosaic virus suggests disruption of PIPO protein impedes movement. Virology 400: 1-7.
23. Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, et al. (2010) Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog 6: e1000962.
24. Gabrenaite-Verkhovskaya R, Andreev IA, Kalinina NO, Torrance L, Taliansky ME, et al. (2008) Cylindrical inclusion protein of potato virus A is associated with a subpopulation of particles isolated from infected plants. J Gen Virol 89: 829-838.
25. Anandalakshmi R, Marathe R, Ge X, Herr JM Jr, Mau C, et al. (2000) A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290: 142-144.
26. Guo D, Spetz C, Saarma M, Valkonen JP, (2003) Two potato proteins, including a novel RING finger protein (HIP1), interact with the potyviral multifunctional protein HCpro. Mol Plant Microbe Interact 16: 405-410.
27. Ballut L, Drucker M, Pugniere M, Cambon F, Blanc S, et al. (2005) HcPro, a multifunctional protein encoded by a plant RNA virus, targets the 20S proteasome and affects its enzymic activities. J Gen Virol 86: 2595-2603.
28. Dielen AS, Sassaki FT, Walter J, Michon T, Menard G, et al. (2011) The 20S proteasome alpha5 subunit of Arabidopsis thaliana carries an RNase activity and interacts in planta with the lettuce mosaic potyvirus HcPro protein. Mol Plant Pathol 12: 137-150.
29. Jin Y, Ma D, Dong J, Li D, Deng C, et al. (2007) The HC-pro protein of potato virus Y interacts with NtMinD of tobacco. Mol Plant Microbe Interact 20: 1505-1511.
30. Cheng YQ, Liu ZM, Xu J, Zhou T, Wang M, 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.
31. Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, et al. (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40: 376-385.
32. Lucas WJ, (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344: 169-184.
33. Vijaya Palani P, Kasiviswanathan V, Chen JC, Chen W, Hsu YH, et al. (2006) The arginine-rich motif of Bamboo mosaic virus satellite RNA-encoded P20 mediates self-interaction, intracellular targeting, and cell-to-cell movement. Molecular plant-microbe interactions: Mol Plant Microbe Interact 19: 758-767.
34. Nagasaki N, Tomioka R, Maeshima M, (2008) A hydrophilic cation-binding protein of Arabidopsis thaliana, AtPCaP1, is localized to plasma membrane via N-myristoylation and interacts with calmodulin and the phosphatidylinositol phosphates PtdIns(3,4,5)P(3) and PtdIns(3,5)P(2). FEBS J 275: 2267-2282.
35. Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ, (2009) An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21: 581-594.
36. Whitham SA, Wang Y, (2004) Roles for host factors in plant viral pathogenicity. Curr Opin Plant Biol 7: 365-371.
37. Lewis JD, Lazarowitz SG, (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci USA 107: 2491-2496.
38. Ide Y, Nagasaki N, Tomioka R, Suito M, Kamiya T, et al. (2007) Molecular properties of a novel, hydrophilic cation-binding protein associated with the plasma membrane. J Exp Bot 58: 1173-1183.
39. Kato M, Nagasaki-Takeuchi N, Ide Y, Tomioka R, Maeshima M, (2010) PCaPs, possible regulators of PtdInsP signals on plasma membrane. Plant Signal Behav 5: 848-850.
40. Ueki S, Spektor R, Natale DM, Citovsky V, (2010) ANK, a host cytoplasmic receptor for the Tobacco mosaic virus cell-to-cell movement protein, facilitates intercellular transport through plasmodesmata. PLoS Pathog 6: e1001201.
41. Furch AC, Zimmermann MR, Will T, Hafke JB, van Bel AJ, (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61: 3697-3708.
42. Dangl JL, Dietrich RA, Richberg MH, (1996) Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell 8: 1793-1807.
43. Otulak K, Garbaczewska G, (2011) Cellular localisation of calcium ions during potato hypersensitive response to Potato virus Y. Micron 42: 381-391.
44. Truniger V, Aranda MA, (2009) Recessive resistance to plant viruses. Adv Virus Res 75: 119-159.
45. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
46. Hayward A, Padmanabhan M, Dinesh-Kumar SP, (2011) Virus-induced gene silencing in nicotiana benthamiana and other plant species. Methods Mol Biol 678: 55-63.
47. Yoo SD, Cho YH, Sheen J, (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572.
48. Jefferson RA, (1987) Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol Biol 5: 387-405.
49. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ, (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.