Phosphatidic Acid Produced by Phospholipase D Promotes RNA Replication of a Plant RNA Virus

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All characterized eukaryotic positive-strand RNA [(+)RNA] viruses replicate their genomes using the viral replication complexes (VRCs), which contain multiple viral and host components, on intracellular membranes. Phospholipids are major constituents of cellular membranes; however, the function(s) of phospholipids in genome replication of (+)RNA viruses remains largely unknown. Here, we show that Red clover necrotic mosaic virus (RCNMV), a plant (+)RNA virus, induces a high accumulation of phosphatidic acid (PA) in infected plant leaves. PA-producing enzymes, phospholipase Dα (PLDα) and PLDβ, are associated with RCNMV VRCs. PA interacts with the viral replication protein and enhances the viral replication by upregulating the activity/assembly of the VRCs in vitro. In summary, RCNMV alters cellular lipid metabolism via PLD to establish a suitable environment for viral replication.

Vyšlo v časopise: Phosphatidic Acid Produced by Phospholipase D Promotes RNA Replication of a Plant RNA Virus. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004909
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004909

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1. den Boon JA, Ahlquist P. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol. 2010; 64: 241–256. doi: 10.1146/annurev.micro.112408.134012 20825348

2. Hyodo K, Kaido M, Okuno T. Host and viral RNA-binding proteins involved in membrane targeting, replication and intercellular movement of plant RNA virus genomes. Front Plant Sci. 2014; 5: Article 321

3. Laliberté JF, Zhang H. Viral manipulation of plant host membranes. Annu Rev Virol. 2014; 1: 237–259.

4. Miller S, Krijnse-Locker J. Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol. 2008; 6: 363–374. doi: 10.1038/nrmicro1890 18414501

5. Mine A, Okuno T. Composition of plant virus RNA replicase complexes. Curr Opin Virol. 2012; 2: 669–675. doi: 10.1016/j.coviro.2012.09.014 23083891

6. Nagy PD, Pogany J. The dependence of viral RNA replication on co-opted host factors. Nat Rev Microbiol. 2012; 10: 137–149. doi: 10.1038/nrmicro2692 22183253

7. Hyodo K, Okuno T. Host factors used by positive-strand RNA plant viruses for genome replication. J. Gen. Plant Pathol. 2014; 80: 123–135.

8. Mandadi KK, Scholthof KB. Plant immune responses against viruses: how does a virus cause disease? Plant Cell. 2013; 25: 1489–1505 doi: 10.1105/tpc.113.111658 23709626

9. Pumplin N, Voinnet O. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol. 2013; 11: 745–760. doi: 10.1038/nrmicro3120 24129510

10. Okuno T, Hiruki C. Molecular biology and epidemiology of Dianthoviruses. Adv Virus Res. 2013; 87: 36–71.

11. Kaido M, Tsuno Y, Mise K, Okuno T. 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. 2009; 395: 232–242. doi: 10.1016/j.virol.2009.09.022 19819513

12. Mine A, Takeda A, Taniguchi T, Taniguchi H, Kaido M, Mise K, et al. Identification and characterization of the 480-kilodalton template-specific RNA-dependent RNA polymerase complex of Red clover necrotic mosaic virus. J Virol. 2010; 84: 6070–6081. doi: 10.1128/JVI.00054-10 20375154

13. Kusumanegara K, Mine A, Hyodo K, Kaido M, Mise K, Okuno T. Identification of domains in p27 auxiliary replicase protein essential for its association with the endoplasmic reticulum membranes in Red clover necrotic mosaic virus. Virology. 2012; 433: 131–141. doi: 10.1016/j.virol.2012.07.017 22898643

14. Turner KA, Sit TL, Callaway AS, Allen NS, Lommel SA. Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology. 2004; 320: 276–290. 15016550

15. Hyodo K, Mine A, Taniguchi T, Kaido M, Mise K, Taniguchi H, et al. ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus. J Virol. 2013; 87: 163–176. doi: 10.1128/JVI.02383-12 23097452

16. Mine A, Hyodo K, Tajima Y, Kusumanegara K, Taniguchi T, Kaido M, et al. Differential roles of Hsp70 and Hsp90 in the assembly of the replicase complex of a positive-strand RNA plant virus. J Virol. 2012; 86: 12091–12104. doi: 10.1128/JVI.01659-12 22933272

17. Hyodo K, Kaido M, Okuno T. Traffic jam on the cellular secretory pathway generated by a replication protein from a plant RNA virus. Plant Signal Behav. 2014; 9: e28644. 24714629

18. Donaldson JG, Jackson CL. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol. 2011; 12: 362–375. doi: 10.1038/nrm3117 21587297

19. Jang JH, Lee CS, Hwang D, Ryu SH. Understanding of the roles of phospholipase D and phosphatidic acid through their binding partners. Prog Lipid Res. 2012; 51: 71–81 doi: 10.1016/j.plipres.2011.12.003 22212660

20. Li M, Hong Y, Wang X. Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta. 2009; 1791: 927–935. doi: 10.1016/j.bbalip.2009.02.017 19289179

21. Testerink C, Munnik T. Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot. 2011; 62: 2349–2361. doi: 10.1093/jxb/err079 21430291

22. Hong Y, Zhang W, Wang X. Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant Cell Environ. 2010; 33: 627–635. doi: 10.1111/j.1365-3040.2009.02087.x 19968827

23. Bargmann BO, Laxalt AM, Riet BT, Schouten E, van Leeuwen W, Dekker HL, et al. LePLDbeta1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J. 2006; 4: 358–368.

24. Kirik A, Mudgett MB. SOBER1 phospholipase activity suppresses phosphatidic acid accumulation and plant immunity in response to bacterial effector AvrBsT. Proc Natl Acad Sci U S A. 2009; 106: 20532–20537. doi: 10.1073/pnas.0903859106 19918071

25. van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G, Boller T, et al. Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol. 2000; 123: 1507–1516. 10938366

26. Yamaguchi T, Minami E, Ueki J, Shibuya N. Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol. 2005; 46: 579–587. 15695430

27. Janda M, Šašek V, Chmelařová H, Andrejch J, Nováková M, Hajšlová J, et al. Phospholipase D affects translocation of NPR1 to the nucleus in Arabidopsis thaliana. Front Plant Sci. 2015; 6: Article 59.

28. Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerström M. Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J. 2006; 47: 947–959. 16925603

29. de Jong CF, Laxalt AM, Bargmann BO, de Wit PJ, Joosten MH, Munnik T. Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J. 2004; 39: 1–12. 15200638

30. Johansson ON, Fahlberg P, Karimi E, Nilsson AK, Ellerström M, Andersson MX. Redundancy among phospholipase D isoforms in resistance triggered by recognition of the Pseudomonas syringae effector AvrRpm1 in Arabidopsis thaliana. Front Plant Sci. 2014; 5: Article 639.

31. Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H, Ellerström M, et al. Arabidopsis phospholipase dδ is involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol. 2013; 163: 896–906. doi: 10.1104/pp.113.223503 23979971

32. Zhang W, Chen J, Zhang H, Song F. Overexpression of a rice diacylglycerol kinase gene OsBIDK1 enhances disease resistance in transgenic tobacco. Mol Cells. 2008; 26: 258–264. 18679055

33. Park J, Gu Y, Lee Y, Yang Z, Lee Y. Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rho-related small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol. 2004; 134: 129–136. 14730067

34. Zhao J, Devaiah SP, Wang C, Li M, Welti R, Wang X. Arabidopsis phospholipase Dβ1 modulates defense responses to bacterial and fungal pathogens. New Phytol. 2013; 199: 228–240. doi: 10.1111/nph.12256 23577648

35. Yamaguchi T, Kuroda M, Yamakawa H, Ashizawa T, Hirayae K, Kurimoto L, et al. Suppression of a Phospholipase D gene, OsPLDβ1, activates defense responses and increases disease resistance in rice. Plant Physiol. 2009; 150: 308–319. doi: 10.1104/pp.108.131979 19286937

36. Canonne J, Froidure-Nicolas S, Rivas S. Phospholipases in action during plant defense signaling. Plant Signal Behav. 2011; 6:13–18. 21248491

37. Brown HA, Gutowski S, Moomaw CR, Slaughter C, Sternweis PC. ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell. 1993; 75: 1137–1144. 8261513

38. Komoda K, Naito S, Ishikawa M. Replication of plant RNA virus genomes in a cell-free extract of evacuolated plant protoplasts. Proc Natl Acad Sci U S A. 2004; 101: 1863–1867. 14769932

39. Wang X, Yan Y, Li Y, Chu X, Wu C, Guo X. GhWRKY40, a Multiple Stress-Responsive Cotton WRKY Gene, Plays an Important Role in the Wounding Response and Enhances Susceptibility to Ralstonia solanacearum Infection in Transgenic Nicotiana benthamiana. PLoS One. 2014; 9: e93577. doi: 10.1371/journal.pone.0093577 24747610

40. Zhu F, Xi DH, Yuan S, Xu F, Zhang DW, Lin HH. Salicylic acid and jasmonic acid are essential for systemic resistance against tobacco mosaic virus in Nicotiana benthamiana. Mol Plant Microbe Interact. 2014; 27: 567–577. doi: 10.1094/MPMI-11-13-0349-R 24450774

41. Nakano M, Nishihara M, Yoshioka H, Takahashi H, Sawasaki T, Ohnishi K, et al. Suppression of DS1 phosphatidic acid phosphatase confirms resistance to Ralstonia solanacearum in Nicotiana benthamiana. PLoS One. 2013; 8: e75124. doi: 10.1371/journal.pone.0075124 24073238

42. Huang PY, Yeh YH, Liu AC, Cheng CP, Zimmerli L. The Arabidopsis LecRK-VI.2 associates with the pattern recognition receptor FLS2 and primes Nicotiana benthamiana pattern-triggered immunity. Plant J. 2014; 79: 243–255 doi: 10.1111/tpj.12557 24844677

43. Munnik T, Arisz SA, De Vrije T, Musgrave A. G Protein Activation Stimulates Phospholipase D Signaling in Plants. Plant Cell. 1995; 7: 2197–2210. 12242371

44. An M, Iwakawa HO, Mine A, Kaido M, Mise K, Okuno T. A Y-shaped RNA structure in the 3' untranslated region together with the trans-activator and core promoter of Red clover necrotic mosaic virus RNA2 is required for its negative-strand RNA synthesis. Virology. 2010; 405: 100–109. doi: 10.1016/j.virol.2010.05.022 20561661

45. Hyodo K, Mine A, Iwakawa HO, Kaido M, Mise K, Okuno T. Identification of amino acids in auxiliary replicase protein p27 critical for its RNA-binding activity and the assembly of the replicase complex in Red clover necrotic mosaic virus. Virology. 2011; 413: 300–309. doi: 10.1016/j.virol.2011.02.017 21440279

46. Iwakawa HO, Kaido M, Mise K, Okuno T. cis-Acting core RNA elements required for negative-strand RNA synthesis and cap-independent translation are separated in the 3'-untranslated region of Red clover necrotic mosaic virus RNA1. Virology. 2007; 369: 168–181. 17727911

47. Iwakawa HO, Mizumoto H, Nagano H, Imoto Y, Takigawa K, Sarawaneeyaruk S, et al. A viral noncoding RNA generated by cis-element-mediated protection against 5'- 3’ RNA decay represses both cap-independent and cap-dependent translation. J Virol. 2008; 82: 10162–10174. doi: 10.1128/JVI.01027-08 18701589

48. Iwakawa HO, Mine A, Hyodo K, An M, Kaido M, Mise K, et al. Template recognition mechanisms by replicase proteins differ between bipartite positive-strand genomic RNAs of a plant virus. J Virol. 2011; 85: 497–509. doi: 10.1128/JVI.01754-10 20980498

49. Mine A, Hyodo K, Takeda A, Kaido M, Mise K, Okuno T. 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. 2010; 407: 213–224. doi: 10.1016/j.virol.2010.07.038 20828775

50. Zhao J. Phospholipase D and phosphatidic acid in plant defence response: from protein–protein and lipid–protein interactions to hormone signalling. J Exp Bot. 2015; 66: 1721–1736. 25680793

51. Chuang C, Barajas D, Qin J, Nagy PD. Inactivation of the host lipin gene accelerates RNA virus replication through viral exploitation of the expanded endoplasmic reticulum membrane. PLoS Pathog. 2014; 10: e1003944. doi: 10.1371/journal.ppat.1003944 24586157

52. Perera R, Riley C, Isaac G, Hopf-Jannasch AS, Moore RJ, Weitz KW, et al. Dengue virus infection perturbs lipid homeostasis in infected mosquito cells. PLoS Pathog. 2012; 8: e1002584. doi: 10.1371/journal.ppat.1002584 22457619

53. Duijsings D, Wessels E, van Emst-de Vries SE Melchers WJ, Willems PH, van Kuppeveld FJ. Reduction of phospholipase D activity during coxsackievirus infection. J Gen Virol. 2007; 88: 3027–3030. 17947526

54. Verheije MH, Raaben M, Mari M, Te Lintelo EG, Reggiori F, van Kuppeveld FJ, et al. Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog. 2008; 4: e1000088. doi: 10.1371/journal.ppat.1000088 18551169

55. Guo L, Wang X. Crosstalk between Phospholipase D and Sphingosine Kinase in Plant Stress Signaling. Front Plant Sci. 2012; 3: Article 51.

56. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, et al. Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell. 2009; 21: 2357–2377. doi: 10.1105/tpc.108.062992 19690149

57. Kim SC, Guo L, Wang X. Phosphatidic acid binds to cytosolic glyceraldehyde-3-phosphate dehydrogenase and promotes its cleavage in Arabidopsis. J Biol Chem. 2013; 288: 11834–11844. doi: 10.1074/jbc.M112.427229 23504314

58. McLoughlin F, Arisz SA, Dekker HL, Kramer G, de Koster CG, Haring MA, et al. Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem J. 2013; 450: 573–581. doi: 10.1042/BJ20121639 23323832

59. Kaido M, Abe K, Mine A, Hyodo K, Taniguchi T, Taniguchi H, et al. GAPDH-A recruits a plant virus movement protein to cortical virus replication complexes to facilitate viral cell-to-cell movement. PLoS Pathog. 2014; 10: e1004505. doi: 10.1371/journal.ppat.1004505 25411849

60. Mizumoto H, Iwakawa H, Kaido M, Mise K, Okuno T. Cap-independent translation mechanism of Red clover necrotic mosaic virus RNA2 differs from that of RNA1 and is linked to RNA replication. J Virol. 2006; 80: 3781–3791 16571795

61. Iwakawa HO, Tajima Y, Taniguchi T, Kaido M, Mise K, Tomari Y, et al. Poly(A)-binding protein facilitates translation of an uncapped/nonpolyadenylated viral RNA by binding to the 3' untranslated region. J Virol. 2012; 86: 7836–7849. doi: 10.1128/JVI.00538-12 22593149

62. Konan KV, Sanchez-Felipe L. Lipids and RNA virus replication. Curr Opin Virol. 2014; 9: 45–52. doi: 10.1016/j.coviro.2014.09.005 25262061

63. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, Proll SC, et al. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog. 2010; 6: e1000719. doi: 10.1371/journal.ppat.1000719 20062526

64. Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, Matula P, et al. Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe. 2011; 9: 32–45. doi: 10.1016/j.chom.2010.12.002 21238945

65. Hirata Y, Ikeda K, Sudoh M, Tokunaga Y, Suzuki A, Weng L, et al. Self-enhancement of hepatitis C virus replication by promotion of specific sphingolipid biosynthesis. PLoS Pathog. 2012; 8: e1002860. doi: 10.1371/journal.ppat.1002860 22916015

66. Weng L, Hirata Y, Arai M, Kohara M, Wakita T, Watashi K, et al. Sphingomyelin activates hepatitis C virus RNA polymerase in a genotype-specific manner. J Virol. 2010; 84: 11761–11770. doi: 10.1128/JVI.00638-10 20844041

67. Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell. 2010; 141: 799–811. doi: 10.1016/j.cell.2010.03.050 20510927

68. Nchoutmboube JA, Viktorova EG, Scott AJ, Ford LA, Pei Z, Watkins PA, et al. Increased long chain acyl-Coa synthetase activity and fatty acid import is linked to membrane synthesis for development of picornavirus replication organelles. PLoS Pathog. 2013; 9: e1003401. doi: 10.1371/journal.ppat.1003401 23762027

69. Belov GA. Modulation of lipid synthesis and trafficking pathways by picornaviruses. Curr Opin Virol. 2014; 9: 19–23. doi: 10.1016/j.coviro.2014.08.007 25240228

70. Pogany J, Nagy PD. Activation of Tomato bushy stunt virus RdRp by cellular Hsp70 is enhanced by phospholipids in vitro. J Virol. 2015; 89: 5714–5723. doi: 10.1128/JVI.03711-14 25762742

71. Takeda A, Tsukuda M, Mizumoto H, Okamoto K, Kaido M, Mise K, et al. A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J. 2005; 24: 3147–3157. 16096641

72. Xiong ZG, Lommel SA. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology. 1991; 182: 388–392. 2024474

73. Janda M, French R, Ahlquist P. High efficiency T7 polymerase synthesis of infectious RNA from cloned brome mosaic virus cDNA and effects of 5' extensions on transcript infectivity. Virology. 1987; 158: 259–262. 18644564

74. Nakasugi K, Crowhurst RN, Bally J, Wood CC, Hellens RP, Waterhouse P. De Novo Transcriptome sequence assembly and analysis of RNA silencing genes of Nicotiana benthamiana. PLoS ONE. 2013; 8: e59534. doi: 10.1371/journal.pone.0059534 23555698

75. Mizumoto H, Tatsuta M, Kaido M, Mise K, Okuno T. Capindependent translational enhancement by the 3' untranslated region of red clover necrotic mosaic virus RNA1. J Virol. 2003; 77: 12113–12121. 14581548

76. Takeda A, Sugiyama K, Nagano H, Mori M, Kaido M, Mise K, et al. Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Lett. 2002; 532: 75–79. 12459466

77. Ratcliff F, Martin-Hernandez AM, Baulcombe DC. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 2001; 25: 237–245. 11169199