A host RNA helicase-like protein, AtRH8, interacts with the potyviral genome-linked protein, VPg, associates with the virus accumulation complex, and is essential for infection

Plant Physiology

Volumn 152, Issue 1, 2010, Pages 255-266

  Huang, Tyng Shyan ^a,b   Wei, Taiyun ^a,b   Laliberté, Jean François ^c   Wang, Aiming ^a,b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; NICOTIANA BENTHAMIANA; POTYVIRUS; PRUNUS; PRUNUS PERSICA;

EID: 73249148517     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.109.147983     Document Type: Article

References (73)

1. Abdul-Razzak A, Guiraud T, Peypelut M, Walter J, Houvenaghel MC, Candresse T, Le Gall O, German-Retana S (2009) Involvement of the cylindrical inclusion (CI) protein in the overcoming of an eIF4E-mediated resistance against Lettuce mosaic potyvirus. Mol Plant Pathol 10: 109-113
2. Ariumi Y, Kuroki M, Abe K, Dansako H, Ikeda M, Wakita T, Kato N (2007) DDX3 DEAD-box RNA helicase is required for Hepatitis C virus RNA replication. J Virol 81: 13922-13926
3. Babu M, Griffiths JS, Huang TS, Wang A (2008) Altered gene expression changes in Arabidopsis leaf tissues and protoplasts in response to Plum pox virus infection. BMC Genomics 9: 325
4. Baulcombe D (2004) RNA silencing in plants. Nature 431: 356-363
5. Beauchemin C, Boutet N, Laliberté JF (2007) Visualization of the interaction between the precursors of VPg, the viral protein linked to the genome of Turnip mosaic virus, and the translation eukaryotic initiation factor (iso) 4E in planta. J Virol 81: 775-782
6. Beauchemin C, Laliberté JF (2007) The poly(A) binding protein is inter nalized in virus-induced vesicles or redistributed to the nucleolus during Turnip mosaic virus infection. J Virol 81: 10905-10913
7. Bruun-Rasmussen M, Moller IS, Tulinius G, Hansen JKR, Lund OS, Johansen IE (2007) The same allele of translation initiation factor 4E mediates resistance against two Potyvirus spp. in Pisum sativum. Mol Plant Microbe Interact 9: 1075-1082
8. Carrington JC, Haldeman R, Dolja VV, Restrepo-Hartwig MA (1993) Internal cleavage and trans-proteolytic activities of the VPg-proteinase (NIa) of tobacco etch potyvirus in vivo. J Virol 67: 6995-7000
9. 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
10. Chung BY, Miller WA, Atkins JF, Firth AE (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci USA 105: 5897-5902
11. Cotton S, Grangeon R, Thuivierge K, Mathieu I, Ide C, Wei T, Wang A, Laliberté JF (2009) Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments and are each derived from a single viral genome. J Virol 83: 10460-10471
12. Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP, García JA, Candresse T, Le Gall O, Revers F (2006) Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Mol Plant Microbe Interact 19: 541-549
13. de la Cruz J, Kressler D, Linder P (1999) Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci 24: 192-198
14. Dufresne PJ, Ubalijoro E, Fortin MG, Laliberté JF (2008) Arabidopsis thaliana class II poly(A)-binding proteins are required for efficient multiplication of Turnip mosaic virus. J Gen Virol 89: 2339-2348
15. Dunoyer P, Thomas C, Harrison S, Revers F, Maule A (2004) A cysteinerich plant protein potentiates potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol 78: 2301-2309
16. Duprat A, Caranta C, Revers F, Menand B, Browning KS, Robaglia C (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32: 927-934
17. Eagles RM, Balmori-Melián E, Beck DL, Gardner RC, Forster RLS (1994) Characterization of NTPase, RNA-binding and RNA helicase activities of the cytoplasmic inclusion protein of tamarillo mosaic potyvirus. Eur J Biochem 224: 677-684
18. Elvira G, Wasiak S, Blandford V, Tong XK, Serrano A, Fan X, del Rayo Sánchez-Carbente M, Servant F, Bell AW, Boismenu D, et al. (2006) Characterization of an RNA granule from developing brain. Mol Cell Proteomics 5: 635-651
19. Fang J, Acheampong E, Dave R, Wang F, Mukhtar M, Pomerantz RJ (2005) The RNA helicase DDX1 is involved in restricted HIV-1 Rev function in human astrocytes. Virology 336: 299-307
20. Fang J, Kubota S, Yang B, Zhou N, Zhang H, Godbout R, Pomerantz RJ (2004) A DEAD box protein facilitates HIV-1 replication as a cellular cofactor of Rev. Virology 330: 471-480
21. Gabrenaite-Verkhovskaya R, Andrew IA, Kalinina NO, Torrance L, Taliansky ME, Makine K (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
22. Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, Maule AJ (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
23. German-Retana S, Walter J, Le Gall O (2008) Lettuce mosaic virus: from pathogen diversity to host interactions. Mol Plant Pathol 9: 127-136
24. Grumet R, Sanford JC, Johnston SA (1987) Pathogen-derived resistance to viral infection using a negative regulatory molecule. Virology 161: 561-569
25. Hafrén A, Makinen K (2008) Purification of viral genome-linked protein VPg from Potato virus A-infected plants reveals several post-transla tionally modified forms of the protein. J Gen Virol 89: 1509-1518
26. Jiang Y, Serviene E, Gal J, Panavas T, Nagy PD (2006) Identification of essential host factors affecting tombusvirus RNA replication based on the yeast Tet promoters Hughes Collection. J Virol 80: 7394-7404
27. Jiménez I, López L, Alamillo JM, Valli A, García JA (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
28. Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005a) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with tobacco etch virus VPg. Plant J 42: 392-405
29. Kang BC, Yeam I, Jahn MM (2005b) Genetics of plant virus resistance. Annu Rev Phytopathol 43: 581-621
30. Kang BC, Yeam I, Li H, Perez KW, Jahn MM (2007) Ectopic expression of a recessive resistance gene generates dominant potyvirus resistance in plants. Plant Biotechnol J 5: 526-536
31. Khan MA, Miyoshi H, Gallie DR, Goss DJ (2008) Potyvirus genomelinked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J Biol Chem 283: 1340-1349
32. Laín S, Martín M, Riechmann JL, García JA (1991) Novel catalytic activity associated with positive-strand RNA virus infection: nucleic acidstimulated ATPase activity of the plum pox potyvirus helicase protein. J Virol 65: 1-6
33. Laín S, Riechmann JL, García JA (1990) RNA helicase: a novel activity associated with a protein encoded by a positive strand RNA virus. Nucleic Acids Res 18: 7003-7006
34. Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-ofsusceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12: 1046-1051
35. Léonard S, Viel C, Beauchemin C, Daigneault N, Fortin MG, Laliberté JF (2004) Interaction of VPg-Pro of Turnip mosaic virus with the translation initiation factor 4E and the poly(A)-binding protein in planta. J Gen Virol 85: 1055-1063
36. Li Z, Pogany J, Panavas T, Xu K, Esposito AM, Kinzy TG, Nagy PD (2009) Translation elongation factor 1A is a component of the tombusvirus replicase complex and affects the stability of the p33 replication cofactor. Virology 385: 245-260
37. Lorsch JR (2002) RNA chaperones exist and DEAD box proteins get a life. Cell 109: 797-800
38. Lu Q, Tang X, Tian G, Wang F, Liu K, Nguyen V, Kohalmi SE, Keller WA, Tsang EWT, Harada JJ, et al. (2009) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J (in press)
39. Maule A, Leh V, Lederer C (2002) The dialogue between viruses and hosts in compatible interactions. Curr Opin Plant Biol 5: 279-284
40. Michon T, Estevez Y, Walter J, German-Retana S, Le Gall O (2006) The potyviral virus genome-linked protein VPg forms a ternary complex with the eukaryotic initiation factors eIF4E and eIF4G and reduces eIF4E affinity for a mRNA cap analogue. FEBS J 273: 1312-1322
41. Mitter N, Sulistyowati E, Grahan MW, Dietzgen RG (2001) Suppression of gene silencing: a threat to virus-resistant transgenic plants? Trends Plant Sci 6: 246-247
42. Mohr S, Stryker JM, Lambowitz AM (2002) A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109: 769-779
43. Moury B, Morel C, Johansen E, Guilbaud L, Souche S, Ayme V, Caranta C, Palloix A, Jacquemond M (2004) Mutations in Potato virus Y genomelinked protein determine virulence toward recessive resistance in Capsicum annuum and Lycopersicon hirsutum. Mol Plant Microbe Interact 17: 322-329
44. Murphy JF, Klein PG, Hunt AG, Shaw JG (1996) Replacement of the tyrosine residue that links a potyviral VPg to the viral RNA is lethal. Virology 220: 535-538
45. Nelson RS, Citovsky V (2005) Plant viruses: invaders of cells and pirates of cellular pathways. Plant Physiol 138: 1809-1814
46. Nicaise V, Gallois JL, Chafiai F, Allen LM, Schurdi-Levraud V, Browning KS, Candresse T, Caranta C, Le Gall O, German-Retana S (2007) Coordinated and selective recruitment of eIF4E and eIF4G factors for potyvirus infection in Arabidopsis thaliana. FEBS Lett 581: 1041-1046
47. Nicaise V, German-Retana S, Sanjuán R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, Le Gall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol 132: 1272-1282
48. Noueiry AO, Chen J, Ahlquist P (2000) A mutant allele of essential, general translation initiation factor DED1 selectively inhibits translation of a viral mRNA. Proc Natl Acad Sci USA 97: 12985-12990
49. Oruetxebarria L, Guo D, Merits A, Makinen K, Saarma M, Valkonen JPT (2001) Identification of the genome-linked protein in virion of Potato virus A, with comparison to other members in the genome Potyvirus. Virus Res 73: 101-112
50. Puustinen P, Makinen K (2004) Uridylylation of the potyvirus VPg by viral replicase NIb correlates with the nucleotide binding capacity of VPg. J Biol Chem 279: 38103-38110
51. Puustinen P, Rajamaki ML, Ivanov KI, Valkonen JPT, Makinen K (2002) Detection of the potyviral genome-linked protein VPg in virions and its phosphorylation by host kinases. J Virol 76: 12703-12711
52. Rajamaki ML, Maki-Valkama T, Makinen K, Valkonen JPT (2004) Infection with potyviruses. In N Talbot, ed, Plant-Pathogen Interactions. Blackwell Publishing, Oxford, pp 68-91
53. Rajamaki ML, Valkonen JPT (2003) Localization of a potyvirus and the viral genome-linked protein in wild potato leaves at an early stage of systemic infection. Mol Plant Microbe Interact 12: 25-34
54. Rajamaki ML, Valkonen JPT (2009) Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Potato virus A in Nicotiana species. Plant Cell 21: 2485-2502
55. Restrepo-Hartwig MA, Carrington JC (1992) Regulation of nuclear transport of a plant potyvirus protein by autoproteolysis. J Virol 66: 5662-5666
56. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11: 40-45
57. Roberts IM, Wang D, Findlay K, Maule AJ (1998) Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (CIs) show that the CI protein acts transiently in aiding virus movement. Virology 245: 173-181
58. Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, Robaglia C, Caranta C (2002) A natural recessive resistance gene against Potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32: 1067-1075
59. Ruffel S, Gallois JL, Lesage ML, Caranta C (2005) The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics 274: 346-353
60. Sato M, Nakahara K, Yoshii M, Ishikawa M, Uyeda I (2005) Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett 579: 1167-1171
61. Schaad MC, Anderberg RJ, Carrington JC (2000) Strain-specific interaction of the Tobacco etch virus NIa protein with the translation initiation factor eIF4E in the yeast two-hybrid system. Virology 273: 300-306
62. Schaad MC, Jensen PE, Carrington JC (1997) Formation of plant RNAvirus replication complexes on membranes: role of an endoplasmic reticulumtargeted viral protein. EMBO J 16: 4049-4059
63. Shand K, Theodoropoulos C, Stenzel D, Dale JL, Harrison M (2009) Expression of Potato virus Y cytoplasmic inclusion protein in tobacco results in disorganization of parenchyma cells, distortion of epidermal cells, and induces mitochondrial and chloroplast abnormalities, formation of membrane whorls and atypical lipid accumulation. Micron 40: 730-736
64. Sparkes IA, Runions J, Kearnes A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1: 2019-2025
65. Tanner NK, Linder P (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 8: 251-262
66. Thivierge K, Cotton S, Dufresne PJ, Mathieu I, Beauchemin C, Ide C, Fortin MG, Laliberté JF (2008) Eukaryotic elongation factor 1A interacts with Turnip mosaic virus RNA-dependent RNA polymerase and VPg-Pro in virus-induced vesicles. Virology 377: 216-225
67. Urcuqui-Inchima S, Haenni AL, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74: 157-175
68. Wang A, Sanfaçon H, Stobbs LW, James D, Thompson D, Svircev AM, Brown DCW (2006) Plum pox virus in Canada: progress in research and future prospects for disease control. Can J Plant Pathol 28: 182-196
69. Wang MB, Metzlaff M (2005) RNA silencing and antiviral defence in plants. Curr Opin Plant Biol 8: 216-222
70. Wei T, Wang A (2008) Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPIand COPII-dependent manner. J Virol 82: 12252-12264
71. Whitham SA, Wang Y (2004) Roles for host factors in plant viral pathogenicity. Curr Opin Plant Biol 7: 365-371
72. Wittmann S, Chatel H, Fortin MG, Laliberté JF (1997) Interaction of the viral protein genome linked of Turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234: 84-92
73. Yedavalli VS, Neuveut C, Chi YH, Kleiman L, Jeang KT (2004) Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 119: 381-392