GAPDH-A Recruits a Plant Virus Movement Protein to Cortical Virus Replication Complexes to Facilitate Viral Cell-to-Cell Movement

English version České info

Intercellular movement of plant viruses is the crucial step during systemic viral infections. Red clover necrotic mosaic virus (RCNMV), a bipartite positive-strand RNA plant virus, forms movement protein (MP)-containing punctate structures on the cortical endoplasmic reticulum in infected cells, which are required for efficient intercellular movement of the virus. We provide evidence that these cortical punctate structures constitute the viral replication complex (VRC), which forms during the early stage of virus infection. Furthermore, we show that a host protein of Nicotiana benthamiana, glyceraldehyde 3-phosphate dehydrogenase-A (NbGAPDH-A), possibly intercalates between the cortical VRC and MP. Knockdown of NbGAPDH-A diffused subcellular localization of MP and reduced intercellular movement of the virus. Chloroplastic NbGAPDH-A relocalized to the cortical VRC after infection with the virus. Our results suggest that the cortical VRC serves not only as the replication factory of viral RNA but also as a transportation hub, which transports viral RNA to neighboring uninfected cells via plasmodesmata.

Vyšlo v časopise: GAPDH-A Recruits a Plant Virus Movement Protein to Cortical Virus Replication Complexes to Facilitate Viral Cell-to-Cell Movement. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004505
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004505

Souhrn

Zdroje

1. den BoonJA, AhlquistP (2010) Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 64: 241–256.

2. den BoonJA, DiazA, AhlquistP (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8: 77–85.

3. LalibertéJF, SanfaçonH (2010) Cellular remodeling during plant virus infection. Annu Rev Phytopathol 48: 69–91.

4. MineA, OkunoT (2012) Composition of plant virus RNA replicase complexes. Curr Opin Virol 2: 669–675.

5. HyodoK, OkunoT (2014) Host factors used by positive-strand RNA plant viruses for genome replication. J Gen Plant Pathol 80: 123–135.

6. HeinleinM, PadgettHS, GensJS, PickardBG, CasperSJ, et al. (1998) Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10: 1107–1120.

7. SzécsiJ, DingXS, LimCO, BendahmaneM, ChoMJ, et al. (1999) Development of tobacco mosaic virus infection sites in Nicotiana benthamiana. Mol Plant Microbe Interact 12: 143–152.

8. DohiK, MoriM, FurusawaI, MiseK, OkunoT (2001) Brome mosaic virus replicase proteins localizes with the movement protein at infection-specific cytoplasmic inclusions in ifected barley leaf cells. Arch Virol 146: 1607–1615.

9. BamunusingheD, HemenwayCL, NelsonRS, SanderfootAA, YeCM, et al. (2009) Analysis of potato virus X replicase and TGBp3 subcellular locations. Virology 393: 272–285.

10. KaidoM, TsunoY, MiseK, OkunoT (2009) Endoplasmic reticulum targeting of the Red clover necrotic mosaic virus movement protein is associated with the replication of viral RNA1 but not that of RNA2. Virology 395: 232–242.

11. MeshiT, WatanabeY, SaitoT, SugimotoA, MaedaT, et al. (1987) Function of the 30 kd protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6: 2557–2563.

12. TatsutaM, MizumotoH, KaidoM, MiseK, OkunoT (2005) The Red clover necrotic mosaic virus RNA2 trans-activator is also a cis-acting RNA2 replication element. J Virol 79: 978–986.

13. WaigmannE, UekiS, TrutnyevaV, CitovskyV (2004) The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. Curr Rev Plant Sci 23: 195–250.

14. LucasWJ (2006) Plant viral movement proteins: Agents for cell-to-cell trafficking of viral genomes. Virology 344: 169–184.

15. HarriesPA, SchoelzJE, NelsonRS (2010) Intracellular transport of viruses and their components: Utilizing the cytoskeleton and membrane highways. Mol Plant Microbe Interact 23: 1381–1393.

16. NiehlA, HeinleinM (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248: 75–99.

17. UekiS, CitovskyV (2011) To gate or not to gate: Regulatory mechanisms for intercellular protein transport and virus movement in plants. Mol Plant 4: 782–793.

18. ChristensenN, TilsnerJ, BellK, HammannP, PartonR, et al. (2009) The 5′ cap of Tobacco mosaic virus (TMV) is required for virion attachment to the actin/endoplasmic reticulum network during early infection. Traffic 10: 536–551.

19. LiuC, NelsonRS (2013) The cell biology of Tobacco mosaic virus replication and movement. Front Plant Sci 4: 12.

20. LiuJ, BlancaflorEB, NelsonRS (2005) The Tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiol 138: 1853–1865.

21. BoykoV, HuQ, SeemanpillaiM, AshbyJ, HeinleinM (2007) Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51: 589–603.

22. SambadeA, BrandnerK, HofmannC, SeemanpillaiM, MuttererJ, et al. (2008) Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 9: 2073–2088.

23. KawakamiS, WatanabeY, BeachyRN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci U S A 101: 6291–6296.

24. HarriesPA, ParkJW, SasakiN, BallardKD, MauleAJ, et al. (2009) Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc Natl Acad Sci U S A 106: 17594–17599.

25. SchoelzJE, HarriesPA, NelsonRS (2011) Intracellular transport of plant viruses: Finding the door out of the cell. Mol Plant 4: 813–831.

26. OkunoT, HirukiC (2013) Molecular biology and epidemiology of dianthoviruses. Adv Virus Res 87: 36–71.

27. TurnerKA, SitTL, CallawayAS, AllenNS, LommelSA (2004) Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology 320: 276–290.

28. MineA, TakedaA, TaniguchiT, TaniguchiH, KaidoM, et al. (2010) Identification and characterization of the 480-kilodalton template-specific RNA-dependent RNA polymerase complex of Red clover necrotic mosaic virus. J Virol 84: 6070–6081.

29. MineA, HyodoK, TakedaA, KaidoM, MiseK, et al. (2010) Interactions between p27 and p88 replicase proteins of Red clover necrotic mosaic virus play an essential role in viral RNA replication and suppression of RNA silencing via the 480-kDa viral replicase complex assembly. Virology 407: 213–224.

30. MineA, HyodoK, TajimaY, KusumanegaraK, TaniguchiT, et al. (2012) Differential roles of Hsp70 and Hsp90 in the assembly of the replicase complex of a positive-strand RNA plant virus. J Virol 86: 12091–12104.

31. HyodoK, MineA, TaniguchiT, KaidoM, MiseK, et al. (2013) ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus. J Virol 87: 163–176.

32. KusumanegaraK, MineA, HyodoK, KaidoM, MiseK, et al. (2012) Identification of domains in p27 auxiliary replicase protein essential for its association with the endoplasmic reticulum membranes in Red clover necrotic mosaic virus. Virology 433: 131–141.

33. LommelSA, Weston-FinaM, XiongZ, LomonossoffGP (1988) The nucleotide sequence and gene organization of red clover necrotic mosaic virus RNA-2. Nucleic Acids Res 16: 8587–8602.

34. XiongZ, KimKH, Giesman-CookmeyerD, LommelSA (1993) The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology 192: 27–32.

35. OsmanTAM, HayesRJ, BuckKW (1992) Cooperative binding of the red clover necrotic mosaic virus movement protein to single-stranded nucleic acids. J Gen Virol 73: 223–227.

36. FujiwaraT, Giesman-CookmeyerD, DingB, LommelSA, LucasWJ (1993) Cell-to-cell trafficking of macromolecules through plasmodesmata potentiated by the red clover necrotic mosaic virus movement protein. Plant Cell 5: 1783–1794.

37. Giesman-CookmyerD, LommelSA (1993) Alanine scanning mutagenesis of a plant virus movement protein identifies three functional domains. Plant Cell 5: 973–982.

38. TremblayD, VaewhongsAA, TurnerKA, SitTL, LommelSA (2005) Cell wall localization of Red clover necrotic mosaic virus movement protein is required for cell-to-cell movement. Virology 333: 10–21.

39. KaidoM, FunatsuN, TsunoY, MiseK, OkunoT (2011) Viral cell-to-cell movement requires formation of cortical punctate structures containing Red clover necrotic mosaic virus movement protein. Virology 413: 205–215.

40. MicheletL, ZaffagniniM, MorisseS, SparlaF, Pérez-PérezME, et al. (2013) Redox regulation of the Calvin-Benson cycle: something old, something new. Front Plant Sci 4: 470.

41. FiggeRM, SchubertM, BrinkmannH, CerffM (1999) Glyceraldehyde-3-phosphate dehydrogenase gene diversity in eubacteria and eukaryotes: evidence for intra- and inter-kingdom gene transfer. Mol Biol Evol 16: 429–440.

42. SitTL, VaewhongsAA, LommelSA (1998) RNA-mediated trans-activation of transcription from a viral RNA. Science 281: 829–832.

43. WeberF, WagnerV, RasmussenSB, HartmannR, PaludanSR (2006) Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 80: 5059–5064.

44. MiorinL, Romero-BreyI, MaiuriP, HoppeS, Krijnse-LockerJ, et al. (2013) Three-dimensional architecture of tick-borne encephalitis virus replication sites and trafficking of the replicated RNA. J Virol 87: 6469–6481.

45. ChoiSH, SeoJ-K, KwonS-J, RaoALN (2012) Helper virus-independent transcription and multimerization of a satellite RNA associated with Cucumber mosaic virus. J Virol 86: 4823–4832.

46. IgarashiA, YamagataK, SugaiT, TakahashiY, SugawaraE, et al. (2009) Apple latent spherical virus vectors for reliable and effective virus-induced gene silencing among a broad range of plants including tobacco, tomato, Arabidopsis thaliana, cucurbits, and legumes. Virology 386: 407–416.

47. JoshiS, PleijCWA, HaenniAL, ChapevilleF, BoschL (1983) Properties of the tobacco mosaic virus intermediate length RNA-2 and its translation. Virology 127: 100–111.

48. WatanabeY, EmoriY, OoshimaI, MeshiT, OhnoT, et al. (1984) Synthesis of TMV-specific RNAs and proteins at the early stage of infection in tobacco protoplast: transient expression of the 30K protein and its mRNA. Virology 133: 18–24.

49. MizumotoH, IwakawaH, KaidoM, MiseK, OkunoT (2006) Cap-independent translation mechanism of Red clover necrotic mosaic virus RNA2 differs from that of RNA1 and is linked to RNA replication. J Virol 80: 3781–3791.

50. TilsnerJ, OparkaKJ (2012) Missing links? – The connection between replication and movement of plant RNA viruses. Curr Opin Virol 2: 705–711.

51. TilsnerJ, LinnikO, LouveauxM, RobertsIM, ChapmanSN, et al. (2013) Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. J Cell Biol 201: 981–995.

52. TilsnerJ, LinnikO, WrightKM, BellK, RobertsAG, et al. (2012) The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol 158: 1359–1370.

53. PriceGD, EvansJR, von CaemmererS, YuJ-W, BadgerMR (1995) Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195: 369–378.

54. MaglieryTJ, WilsonCGM, PanW, MishlerD, GhoshI, et al. (2005) Detecting protein-protein interactions with a green fluorescent protein fragment reassembly trap: scope and mechanism. J Am Chem Soc 127: 146–157.

55. OkamotoK, NaganoH, IwakawaH, MizumotoH, TakedaA, et al. (2008) cis-Preferential requirement of a −1 frameshift product p88 for the replication of Red clover necrotic mosaic virus RNA1. Virology 375: 205–212.

56. IwakawaH-O, MineA, HyodoK, AnM, KaidoM, et al. (2011) Template recognition mechanism by replicase proteins differ between bipartite positive-strand genomic RNAs of a plant virus. J Virol 85: 497–509.

57. WangRY-L, NagyPD (2008) Tomato bushy stunt virus co-opts the RNA-binding function of a host metabolic enzyme for viral genomic RNA synthesis. Cell Host Microbe 3: 178–187.

58. PrasanthKR, HuangY-W, LiouM-R, WangRY-L, HuC-C, et al. (2011) Glyceraldehyde 3-phosphate dehydrogenase negatively regulates the replication of Bamboo mosaic virus and its associated satellite RNA. J Virol 85: 8829–8840.

59. ShihM-C, LazarG, GoodmanHM (1986) Evidence in favor of the symbiotic origin of chloroplasts: Primary structure and evolution of tobacco glyceraldehyde-3-phophate dehydrogenase. Cell 47: 73–80.

60. LinS-S, ChangSC, WangY-H, SunC-Y, ChangM-F (2000) Specific interaction between the Hepatitis delta virus RNA and glyceraldehyde 3-phophate dehydrogenase: An enhancement on ribozyme catalysis. Virology 271: 46–57.

61. SiroverMA (1999) New insight into an old protein: The functional diversity of mammalian glyceraldehyde-3- phosphate dehydrogenase. Biochim Biophys Acta 1432: 159–184.

62. SiroverMA (2005) New nuclear functions of the glycolytic protein, glyceraldehyde-3- phosphate dehydrogenase, in mammalian cells. J Cell Biochem 95: 45–52.

63. HuangY-W, HuC-C, LinN-S, HsuY-H (2012) Unusual roles of host metabolic enzymes and housekeeping proteins in plant virus replication. Curr Opin Virol 2: 676–682.

64. LinJ-W, DingM-P, HsuY-H, TsaiC-H (2007) Chloroplast phosphoglycerate kinase, a gluconeogenetic enzyme, is required for efficient accumulation of Bamboo mosaic virus. Nucl Acids Res 35: 424–432.

65. ChengS-F, HuangY-P, ChenL-H, HsuY-H, TsaiC-H (2013) Chloroplast phosphoglycerate kinase is involved in the targeting of Bamboo mosaic virus to chloroplasts in Nicotiana benthamiana plants. Plant Physiol 163: 1598–1608.

66. BhatS, FolimonovaSF, ColeAB, BallardKD, LeiZ, et al. (2013) Influence of host chloroplast proteins on Tobacco mosaic virus accumulation and intercellular movement. Plant Physiol 161: 134–147.

67. TakedaA, TsukudaM, MizumotoH, OkamotoK, KaidoM, et al. (2005) A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J 24: 3147–3157.

68. XiongZG, LommelSA (1991) Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology 182: 388–392.

69. MitsuharaI, UgakiM, HirochikaH, OhshimaM, MurakamiT, et al. (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol 37: 49–59.

70. TamaiA, MeshiT (2001) Tobamoviral movement protein transiently expressed in a single epidermal cell functions beyond multiple plasmodesmata and spreads multicellularly in an infection-coupled manner. Mol Plant Microbe Interact 14: 126–134.

71. HamamotoH, SugiyamaY, NakagawaN, HashidaE, MatsunagaY, et al. (1993) A new tobacco mosaic virus vector and its use for the systemic production of angiotensin-I-converting enzyme inhibitor in transgenic tobacco and tomato. Nature Biotech 11: 930–932.

72. KaidoM, MoriM, MiseK, OkunoT, FurusawaI (1997) Auto-cleavable ribozyme sequence attached to brome mosaic virus cDNAs enhances accumulation of viral RNAs transcribed in vivo from the cDNAs. Ann Phytopathol Soc Jpn 63: 95–98.

73. LiJ-F, ChungHS, NiuY, BushJ, McCormackM, et al. (2013) Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants. Plant Cell 25: 1507–1522.

74. Navas-CastilloJ, Albiach-MartiMR, GowdaS, HilfME, GarnseySM, et al. (1997) Kinetics of accumulation of citrus tristeza virus RNAs. Virology 228: 92–97.

75. KawaiT, GonoiA, NittaM, KaidoM, YamagishiN, et al. (2014) Virus-induced gene silencing in Apricot (Prunus armeniaca L.) and Japanese apricot (P. mume Siebold & Zucc.) with the Apple latent spherical virus vector system. J Jpn Soc Hort Sci 83: 23–31.

76. MizumotoH, TatsutaM, KaidoM, MiseK, OkunoT (2003) Cap-independent translational enhancement by the 3′ untranslated region of Red clover necrotic mosaic virus RNA1. J Virol 77: 12113–12121.