Chloroplast phosphoglycerate kinase is involved in the targeting of Bamboo mosaic virus to chloroplasts in Nicotiana benthamiana plants

Plant Physiology

Volumn 163, Issue 4, 2013, Pages 1598-1608

  Cheng, Shun Fang ^a   Huang, Ying Ping ^a   Chen, Li Hung ^a   Hsu, Yau Heiu ^a,b   Tsai, Ching Hsiu ^a,b  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; PHOSPHOGLYCERATE KINASE; RNA BINDING PROTEIN; VEGETABLE PROTEIN; VIRUS RNA;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; CHLOROPLAST; DOMINANT GENE; DOWN REGULATION; ENZYMOLOGY; GENE SILENCING; INTRACELLULAR SPACE; METABOLISM; MOLECULAR GENETICS; MOSAIC VIRUS; PHYSIOLOGY; RNA TRANSPORT; SEQUENCE ALIGNMENT; TOBACCO; TRANSPORT AT THE CELLULAR LEVEL; VIROLOGY; VIRUS REPLICATION;

AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; CAPSID PROTEINS; CHLOROPLASTS; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; GENES, DOMINANT; INTRACELLULAR SPACE; MOLECULAR SEQUENCE DATA; MOSAIC VIRUSES; PHOSPHOGLYCERATE KINASE; PLANT PROTEINS; RNA TRANSPORT; RNA, VIRAL; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; TOBACCO; VIRUS REPLICATION;

EID: 84888856728     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.229666     Document Type: Article

References (54)

1. Ahlquist P, Noueiry AO, Lee WM, Kushner DB, Dye BT (2003) Host factors in positive-strand RNA virus genome replication. J Virol 77: 8181-8186
2. Bamunusinghe D, Hemenway CL, Nelson RS, Sanderfoot AA, Ye CM, Silva MA, Payton M, Verchot-Lubicz J (2009) Analysis of potato virus X replicase and TGBp3 subcellular locations. Virology 393: 272-285
3. Banks RD, Blake CC, Evans PR, Haser R, Rice DW, Hardy GW, Merrett M, Phillips AW (1979) Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. Nature 279: 773-777
4. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM (1998) Localization of ASH1mRNA particles in living yeast. Mol Cell 2: 437-445
5. Carette JE, Stuiver M, Van Lent J, Wellink J, Van Kammen A (2000) Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J Virol 74: 6556-6563
6. Chen IH, Chiu MH, Cheng SF, Hsu YH, Tsai CH (2013) The glutathione transferase of Nicotiana benthamiana NbGSTU4 plays a role in regulating the early replication of Bamboo mosaic virus. New Phytol 199: 749-757
7. Chen IH, Chou WJ, Lee PY, Hsu YH, Tsai CH (2005) The AAUAAA motif of Bamboo mosaic virus RNA is involved in minus-strand RNA synthesis and plus-strand RNA polyadenylation. J Virol 79: 14555-14561
8. Cheng JH, Ding MP, Hsu YH, Tsai CH (2001) The partial purified RNAdependent RNA polymerases from Bamboo mosaic potexvirus and Potato virus X infected plants containing the template-dependent activities. Virus Res 80: 41-52
9. Cheng SF, Tsai MS, Huang CL, Huang YP, Chen IH, Lin NS, Hsu YH, Tsai CH, Cheng CP (2013) Ser/Thr kinase-like protein of Nicotiana benthamiana is involved in the cell-to-cell movement of Bamboo mosaic virus. PLoS ONE 8: e62907
10. Chiu MH, Chen IH, Baulcombe DC, Tsai CH (2010) The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol Plant Pathol 11: 641-649
11. Cowan GH, Roberts AG, Chapman SN, Ziegler A, Savenkov EI, Torrance L (2012) The Potato mop-top virus TGB2 protein and viral RNA associate with chloroplasts and viral infection induces inclusions in the plastids. Front Plant Sci 3: 290
12. Cruz SS, Roberts AG, Prior DA, Chapman S, Oparka KJ (1998) Cell-to-cell and phloem-mediated transport of Potato virus X. The role of virions. Plant Cell 10: 495-510
13. Fouts DE, True HL, Celander DW (1997) Functional recognition of fragmented operator sites by R17/MS2 coat protein, a translational repressor. Nucleic Acids Res 25: 4464-4473
14. Gancarz BL, Hao L, He Q, Newton MA, Ahlquist P (2011) Systematic identification of novel, essential host genes affecting bromovirus RNA replication. PLoS ONE 6: e23988
15. Han S, Sanfaçon H (2003) Tomato ringspot virus proteins containing the nucleoside triphosphate binding domain are transmembrane proteins that associate with the endoplasmic reticulum and cofractionate with replication complexes. J Virol 77: 523-534
16. Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci USA 94: 2122-2127
17. Herold J, Andino R (2001) Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol Cell 7: 581-591
18. Huang YL, Han YT, Chang YT, Hsu YH, Meng M (2004) Critical residues for GTP methylation and formation of the covalent m7GMP-enzyme intermediate in the capping enzyme domain of Bamboo mosaic virus. J Virol 78: 1271-1280
19. Huang YW, Hu CC, Liou MR, Chang BY, Tsai CH, Meng MH, Lin NS, Hsu YH (2012) Hsp90 interacts specifically with viral RNA and differentially regulates replication initiation of Bamboo mosaic virus and associated satellite RNA. PLoS Pathog 8: e1002726
20. Ishikawa M, Díez J, Restrepo-Hartwig M, Ahlquist P (1997) Yeast mutations in multiple complementation groups inhibit brome mosaic virus RNA replication and transcription and perturb regulated expression of the viral polymerase-like gene. Proc Natl Acad Sci USA 94: 13810-13815
21. Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 101: 6291-6296
22. Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P (2003) Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci USA 100: 15764-15769
23. Laliberté JF, Sanfaçon H (2010) Cellular remodeling during plant virus infection. Annu Rev Phytopathol 48: 69-91
24. Li CY, Zhang K, Zeng XW, Jackson S, Zhou Y, Hong YG (2009a) A cis element within flowering locus T mRNA determines its mobility and facilitates trafficking of heterologous viral RNA. J Virol 83: 3540-3548
25. Li YI, Chen YJ, Hsu YH, MengM(2001a) Characterization of the AdoMetdependent guanylyltransferase activity that is associated with the N terminus of Bamboo mosaic virus replicase. J Virol 75: 782-788
26. Li YI, Cheng YM, Huang YL, Tsai CH, Hsu YH, Meng M (1998) Identification and characterization of the Escherichia coli-expressed RNAdependent RNA polymerase of Bamboo mosaic virus. J Virol 72: 10093-10099
27. Li YI, Shih TW, Hsu YH, Han YT, Huang YL, Meng M (2001b) The helicase-like domain of plant potexvirus replicase participates in formation of RNA 5' cap structure by exhibiting RNA 5'-triphosphatase activity. J Virol 75: 12114-12120
28. Li ZH, Pogany J, Panavas T, Xu K, Esposito AM, Kinzy TG, Nagy PD (2009b) Translation elongation factor 1A is a component of the tombusvirus replicase complex and affects the stability of the p33 replication co-factor. Virology 385: 245-260
29. Lin JW, Ding MP, Hsu YH, Tsai CH (2007) Chloroplast phosphoglycerate kinase, a gluconeogenetic enzyme, is required for efficient accumulation of Bamboo mosaic virus. Nucleic Acids Res 35: 424-432
30. Lin MK, Chang BY, Liao JT, Lin NS, Hsu YH (2004) Arg-16 and Arg-21 in the N-terminal region of the triple-gene-block protein 1 of Bamboo mosaic virus are essential for virus movement. J Gen Virol 85: 251-259
31. Lin MK, Hu CC, Lin NS, Chang BY, Hsu YH (2006) Movement of potexviruses requires species-specific interactions among the cognate triple gene block proteins, as revealed by a trans-complementation assay based on the Bamboo mosaic virus satellite RNA-mediated expression system. J Gen Virol 87: 1357-1367
32. Lin NS, Chen CC, Hsu YH (1993) Post-embedding in situ hybridization for localization of viral nucleic acid in ultra-thin sections. J Histochem Cytochem 41: 1513-1519
33. Lin NS, Lin BY, Lo NW, Hu CC, Chow TY, Hsu YH (1994) Nucleotide sequence of the genomic RNA of Bamboo mosaic potexvirus. J Gen Virol 75: 2513-2518
34. Mas A, Alves-Rodrigues I, Noueiry A, Ahlquist P, Díez J (2006) Host deadenylation-dependent mRNA decapping factors are required for a key step in Brome mosaic virus RNA replication. J Virol 80: 246-251
35. McCartney AW, Greenwood JS, Fabian MR, White KA, Mullen RT (2005) Localization of the Tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 17: 3513-3531
36. McHarg J, Kelly SM, Price NC, Cooper A, Littlechild JA (1999) Sitedirected mutagenesis of proline 204 in the 'hinge' region of yeast phosphoglycerate kinase. Eur J Biochem 259: 939-945
37. Mochizuki T, Hirai K, Kanda A, Ohnishi J, Ohki T, Tsuda S (2009) Induction of necrosis via mitochondrial targeting of Melon necrotic spot virus replication protein p29 by its second transmembrane domain. Virology 390: 239-249
38. Nagy PD, Pogany J (2008) Multiple roles of viral replication proteins in plant RNA virus replication. Methods Mol Biol 451: 55-68
39. Nishikiori M, Dohi K, Mori M, Meshi T, Naito S, Ishikawa M (2006) Membrane-bound Tomato mosaic virus replication proteins participate in RNA synthesis and are associated with host proteins in a pattern distinct from those that are not membrane bound. J Virol 80: 8459-8468
40. Panavas T, Serviene E, Brasher J, Nagy PD (2005) Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc Natl Acad Sci USA 102: 7326-7331
41. Patarroyo C, Laliberté JF, Zheng H (2012) Hijack it, change it: how do plant viruses utilize the host secretory pathway for efficient viral replication and spread? Front Plant Sci 3: 308
42. Pathak KB, Sasvari Z, Nagy PD (2008) The host Pex19p plays a role in peroxisomal localization of tombusvirus replication proteins. Virology 379: 294-305
43. Pogany J, Stork J, Li Z, Nagy PD (2008) In vitro assembly of the Tomato bushy stunt virus replicase requires the host Heat shock protein 70. Proc Natl Acad Sci USA 105: 19956-19961
44. Prod'homme D, Jakubiec A, Tournier V, Drugeon G, Jupin I (2003) Targeting of the Turnip yellow mosaic virus 66K replication protein to the chloroplast envelope is mediated by the 140K protein. J Virol 77: 9124-9135
45. Schaad MC, Jensen PE, Carrington JC (1997) Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J 16: 4049-4059
46. Tsai CH, Cheng CP, Peng CW, Lin BY, Lin NS, Hsu YH (1999) Sufficient length of a poly(A) tail for the formation of a potential pseudoknot is required for efficient replication of Bamboo mosaic potexvirus RNA. J Virol 73: 2703-2709
47. Valegârd K, Murray JB, Stonehouse NJ, van den Worm S, Stockley PG, Liljas L (1997) The three-dimensional structures of two complexes between recombinant MS2 capsids and RNA operator fragments reveal sequence-specific protein-RNA interactions. J Mol Biol 270: 724-738
48. Vijaya Palani P, Kasiviswanathan V, Chen JC, Chen W, Hsu YH, Lin NS (2006) The arginine-rich motif of Bamboo mosaic virus satellite RNAencoded P20 mediates self-interaction, intracellular targeting, and cellto-cell movement. Mol Plant Microbe Interact 19: 758-767
49. Waggoner S, Sarnow P (1998) Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirusinfected cells. J Virol 72: 6699-6709
50. Walter BL, Parsley TB, Ehrenfeld E, Semler BL (2002) Distinct poly(rC) binding protein KH domain determinants for poliovirus translation initiation and viral RNA replication. J Virol 76: 12008-12022
51. Wei T, Huang TS, McNeil J, Laliberté JF, Hong J, Nelson RS, Wang A (2010) Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J Virol 84: 799-809
52. Yamanaka T, Ohta T, TakahashiM, Meshi T, Schmidt R, Dean C, Naito S, Ishikawa M (2000) TOM1, an Arabidopsis gene required for efficient multiplication of a tobamovirus, encodes a putative transmembrane protein. Proc Natl Acad Sci USA 97: 10107-10112
53. Yang CC, Liu JS, Lin CP, Lin LS (1997) Nucleotide sequence and phylogenetic analysis of a bamboo mosaic potexvirus isolated from common bamboo (Bambusa vulgaris McClure). Bot Bull Acad Sin 38: 77-84
54. Zhang F, Simon AE (2003) A novel procedure for the localization of viral RNAs in protoplasts and whole plants. Plant J 35: 665-673