Skip to main content

Advertisement

SpringerLink
Log in

Host factors used by positive-strand RNA plant viruses for genome replication

  • REVIEW FOR THE 100TH ANNIVERSARY
  • Published:
Journal of General Plant Pathology Aims and scope Submit manuscript

Abstract

Replication of positive-strand RNA [(+)RNA] viruses proceeds through well-orchestrated actions of both viral and host factors. Remarkable features of eukaryotic (+)RNA virus replication include hijacking of host factors by viral components and remodeling of intracellular membranes to establish the viral replication factory, where viral RNA is synthesized. Here we review recent progress in our understanding of how (+)RNA plant viruses use host factors to create favorable environments for viral RNA replication.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Asano M, Satoh R, Mochizuki A, Tsuda S, Yamanaka T, Nishiguchi M, Hirai K, Meshi T, Naito S, Ishikawa M (2005) Tobamovirus-resistant tobacco generated by RNA interference directed against host genes. FEBS Lett 579:4479–4484

    CAS  PubMed  Google Scholar 

  • Barajas D, Nagy PD (2010) Ubiquitination of tombusvirus p33 replication protein plays a role in virus replication and binding to the host Vps23p ESCRT protein. Virology 397:358–368

    CAS  PubMed Central  PubMed  Google Scholar 

  • Barajas D, Jiang Y, Nagy PD (2009) A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog 5:e1000705

    PubMed Central  PubMed  Google Scholar 

  • Bassham DC, Blatt MR (2008) SNAREs: cogs and coordinators in signaling and development. Plant Physiol 147:1504–1515

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beckham CJ, Light HR, Nissan TA, Ahlquist P, Parker R, Noueiry A (2007) Interactions between brome mosaic virus RNAs and cytoplasmic processing bodies. J Virol 81:9759–9768

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buck KW (1996) Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv Virus Res 47:159–251

    CAS  PubMed  Google Scholar 

  • Camborde L, Planchais S, Tournier V, Jakubiec A, Drugeon G, Lacassagne E, Pflieger S, Chenon M, Jupin I (2010) The ubiquitin-proteasome system regulates the accumulation of Turnip yellow mosaic virus RNA-dependent RNA polymerase during viral infection. Plant Cell 22:3142–3152

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Castorena KM, Stapleford KA, Miller DJ (2010) Complementary transcriptomic, lipidomic, and targeted functional genetic analyses in cultured Drosophila cells highlight the role of glycerophospholipid metabolism in Flock House virus RNA replication. BMC Genom 11:183

    Google Scholar 

  • Chen J, Ahlquist P (2000) Brome mosaic virus polymerase-like protein 2a is directed to the endoplasmic reticulum by helicase-like viral protein 1a. J Virol 74:4310–4318

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J, Noueiry A, Ahlquist P (2001) Brome mosaic virus Protein 1a recruits viral RNA2 to RNA replication through a 5′ proximal RNA2 signal. J Virol 75:3207–3219

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen Z, Zhou T, Wu X, Hong Y, Fan Z, Li H (2008) Influence of cytoplasmic heat shock protein 70 on viral infection of Nicotiana benthamiana. Mol Plant Pathol 9:809–817

    CAS  PubMed  Google Scholar 

  • Chen CE, Yeh KC, Wu SH, Wang HI, Yeh HH (2013a) A vicilin-like seed storage protein, PAP85, is involved in Tobacco mosaic virus replication. J Virol 87:6888–6900

    PubMed Central  PubMed  Google Scholar 

  • Chen IH, Chiu MH, Cheng SF, Hsu YH, Tsai CH (2013b) The glutathione transferase of Nicotiana benthamiana NbGSTU4 plays a role in regulating the early replication of Bamboo mosaic virus. New Phytol 199:749–757

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng SF, Huang YP, Wu ZR, Hu CC, Hsu YH, Tsai CH (2010) Identification of differentially expressed genes induced by Bamboo mosaic virus infection in Nicotiana benthamiana by cDNA-amplified fragment length polymorphism. BMC Plant Biol 10:286

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chenon M, Camborde L, Cheminant S, Jupin I (2012) A viral deubiquitylating enzyme targets viral RNA-dependent RNA polymerase and affects viral infectivity. EMBO J 31:741–753

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen P (2000) The regulation of protein function by multisite phosphorylation—a 25 year update. Trends Biochem Sci 25:596–601

    CAS  PubMed  Google Scholar 

  • Coller J, Parker R (2004) Eukaryotic mRNA decapping. Annu Rev Biochem 73:861–890

    CAS  PubMed  Google Scholar 

  • Cotton S, Grangeon R, Thivierge 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • D’Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7:347–358

    PubMed  Google Scholar 

  • den Boon JA, Ahlquist P (2010) Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 64:241–256

    Google Scholar 

  • den Boon JA, Diaz A, Ahlquist P (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8:77–85

    Google Scholar 

  • Diaz A, Wang X, Ahlquist P (2010) Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc Natl Acad Sci USA 107:16291–16296

    CAS  PubMed Central  PubMed  Google Scholar 

  • Díez J, Ishikawa M, Kaido M, Ahlquist P (2000) Identification and characterization of a host protein required for efficient template selection in viral RNA replication. Proc Natl Acad Sci USA 97:3913–3918

    PubMed Central  PubMed  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:reviews3004.1–3004.10

    Google Scholar 

  • Donaldson JG, Jackson CL (2011) ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 12:362–375

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dreher TW, Miller WA (2006) Translational control in positive strand RNA plant viruses. Virology 344:185–197

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dreher TW, Uhlenbeck OC, Browning KS (1999) Quantitative assessment of EF-1α GTP binding to aminoacyl-tRNAs, aminoacyl-viral RNA, and tRNA shows close correspondence to the RNA binding properties of EF-Tu. J Biol Chem 274:666–672

    CAS  PubMed  Google Scholar 

  • Dufresne PJ, Thivierge K, Cotton S, Beauchemin C, Ide C, Ubalijoro E, Laliberté JF, Fortin MG (2008) Heat shock 70 protein interaction with Turnip mosaic virus RNA-dependent RNA polymerase within virus-induced membrane vesicles. Virology 374:217–227

    CAS  PubMed  Google Scholar 

  • Fodor J, Hideg E, Kecskés A, Király Z (2001) In vivo detection of tobacco mosaic virus-induced local and systemic oxidative burst by electron paramagnetic resonance spectroscopy. Plant Cell Physiol 42:775–779

    CAS  PubMed  Google Scholar 

  • Fujisaki K, Ishikawa M (2008) Identification of an Arabidopsis thaliana protein that binds to tomato mosaic virus genomic RNA and inhibits its multiplication. Virology 380:402–411

    CAS  PubMed  Google Scholar 

  • Galão RP, Chari A, Alves-Rodrigues I, Lobão D, Mas A, Kambach C, Fischer U, Díez J (2010) LSm1-7 complexes bind to specific sites in viral RNA genomes and regulate their translation and replication. RNA 16:817–827

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hafrén A, Hofius D, Rönnholm G, Sonnewald U, Mäkinen K (2010) HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. Plant Cell 22:523–535

    PubMed Central  PubMed  Google Scholar 

  • Hagiwara Y, Komoda K, Yamanaka T, Tamai A, Meshi T, Funada R, Tsuchiya T, Naito S, Ishikawa M (2003) Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. EMBO J 22:344–353

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haruna I, Spiegelman S (1965) Autocatalytic synthesis of a viral RNA in vitro. Science 150:884–886

    CAS  PubMed  Google Scholar 

  • Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I, Millar AH (2007) SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Res 35:D213–D218

    CAS  PubMed Central  PubMed  Google Scholar 

  • Héricourt F, Blanc S, Redeker V, Jupin I (2000) Evidence for phosphorylation and ubiquitinylation of the turnip yellow mosaic virus RNA-dependent RNA polymerase domain expressed in a baculovirus-insect cell system. Biochem J 349:417–425

    PubMed Central  PubMed  Google Scholar 

  • Hernández JA, Rubio M, Olmos E, Ros-Barceló A, Martínez-Gómez P (2004) Oxidative stress induced by long-term plum pox virus infection in peach (Prunus persica). Physiol Plant 122:486–495

    Google Scholar 

  • Hernández JA, Díaz-Vivancos P, Rubio M, Olmos E, Ros-Barceló A, Martínez-Gómez P (2006) Long-term plum pox virus infection produces an oxidative stress in a susceptible apricot, Prunus armeniaca, cultivar but not in a resistant cultivar. Physiol Plant 126:140–152

    Google Scholar 

  • Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, Pau C, van der Schaar H, Kaushik-Basu N, Balla T, Cameron CE, Ehrenfeld E, van Kuppeveld FJ, Altan-Bonnet N (2010) Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:799–811

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huang TS, Nagy PD (2011) Direct inhibition of tombusvirus plus-strand RNA synthesis by a dominant negative mutant of a host metabolic enzyme, glyceraldehyde-3-phosphate dehydrogenase, in yeast and plants. J Virol 85:9090–9102

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huang TS, Wei T, Laliberté JF, Wang A (2010) 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 Physiol 152:255–266

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huang YW, Hu CC, Lin NS, Hsu YH (2012a) Unusual roles of host metabolic enzymes and housekeeping proteins in plant virus replication. Curr Opin Virol 2:676–682

    CAS  PubMed  Google Scholar 

  • Huang YW, Hu CC, Liou MR, Chang BY, Tsai CH, Meng M, Lin NS, Hsu YH (2012b) Hsp90 interacts specifically with viral RNA and differentially regulates replication initiation of Bamboo mosaic virus and associated satellite RNA. PLoS Pathog 8:e1002726

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hwang J, Oh CS, Kang BC (2013) Translation elongation factor 1B (eEF1B) is an essential host factor for Tobacco mosaic virus infection in plants. Virology 439:105–114

    CAS  PubMed  Google Scholar 

  • Hyodo K, Mine A, Iwakawa HO, Kaido M, Mise K, Okuno T (2011) 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 413:300–309

    CAS  PubMed  Google Scholar 

  • Hyodo K, Mine A, Taniguchi T, Kaido M, Mise K, Taniguchi H, Okuno T (2013) ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus. J Virol 87:163–176

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ishibashi K, Miyashita S, Katoh E, Ishikawa M (2012) Host membrane proteins involved in the replication of tobamovirus RNA. Curr Opin Virol 2:699–704

    CAS  PubMed  Google Scholar 

  • Ishikawa M, Okada Y (2004) Replication of tobamovirus RNA. Proc Jpn Acad Ser B 80:215–224

    CAS  Google Scholar 

  • Iwakawa HO, Mine A, Hyodo K, An M, Kaido M, Mise K, Okuno T (2011) Template recognition mechanisms by replicase proteins differ between bipartite positive-strand genomic RNAs of a plant virus. J Virol 85:497–509

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iwakawa HO, Tajima Y, Taniguchi T, Kaido M, Mise K, Tomari Y, Taniguchi H, Okuno T (2012) Poly(A)-binding protein facilitates translation of an uncapped/nonpolyadenylated viral RNA by binding to the 3′ untranslated region. J Virol 86:7836–7849

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jaag HM, Pogany J, Nagy PD (2010) A host Ca2+/Mn2+ ion pump is a factor in the emergence of viral RNA recombinants. Cell Host Microbe 7:74–781

    CAS  PubMed  Google Scholar 

  • Jakubiec A, Jupin I (2007) Regulation of positive-strand RNA virus replication: the emerging role of phosphorylation. Virus Res 129:73–79

    CAS  PubMed  Google Scholar 

  • Jakubiec A, Tournier V, Drugeon G, Pflieger S, Camborde L, Vinh J, Héricourt F, Redeker V, Jupin I (2006) Phosphorylation of viral RNA-dependent RNA polymerase and its role in replication of a plus-strand RNA virus. J Biol Chem 281:21236–21249

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kang HK, Yang SH, Lee YP, Park YI, Kim SH (2012) A tobacco CBL-interacting protein kinase homolog is involved in phosphorylation of the N-terminal domain of the cucumber mosaic virus polymerase 2a protein. Biosci Biotechnol Biochem 76:2101–2106

    CAS  PubMed  Google Scholar 

  • Kim SH, Palukaitis P, Park YI (2002) Phosphorylation of cucumber mosaic virus RNA polymerase 2a protein inhibits formation of replicase complex. EMBO J 21:2292–2300

    CAS  PubMed Central  PubMed  Google Scholar 

  • Komoda K, Mawatari N, Hagiwara-Komoda Y, Naito S, Ishikawa M (2007) Identification of a ribonucleoprotein intermediate of tomato mosaic virus RNA replication complex formation. J Virol 81:2584–2591

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kovalev N, Barajas D, Nagy PD (2012a) Similar roles for yeast Dbp2 and Arabidopsis RH20 DEAD-box RNA helicases to Ded1 helicase in tombusvirus plus-strand synthesis. Virology 432:470–484

    CAS  PubMed  Google Scholar 

  • Kovalev N, Pogany J, Nagy PD (2012b) A Co-Opted DEAD-Box RNA helicase enhances tombusvirus plus-strand synthesis. PLoS Pathog 8:e1002537

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kusumanegara K, Mine A, Hyodo K, Kaido M, Mise K, Okuno T (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

    CAS  PubMed  Google Scholar 

  • Laliberté JF, Sanfaçon H (2010) Cellular remodeling during plant virus infection. Annu Rev Phytopathol 48:69–91

    PubMed  Google Scholar 

  • Lee WM, Ahlquist P (2003) Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J Virol 77:12819–12828

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee WM, Ishikawa M, Ahlquist P (2001) Mutation of host ∆9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J Virol 75:2097–2106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Z, Barajas D, Panavas T, Herbst DA, Nagy PD (2008) Cdc34p ubiquitin-conjugating enzyme is a component of the tombusvirus replicase complex and ubiquitinates p33 replication protein. J Virol 82:6911–6926

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 co-factor. Virology 385:245–260

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Z, Pogany J, Tupman S, Esposito AM, Kinzy TG, Nagy PD (2010) Translation elongation factor 1A facilitates the assembly of the tombusvirus replicase and stimulates minus-strand synthesis. PLoS Pathog 6:e1001175

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23:147–174

    CAS  PubMed  Google Scholar 

  • Liu L, Westler WM, den Boon JA, Wang X, Diaz A, Steinberg HA, Ahlquist P (2009) An amphipathic α-helix controls multiple roles of brome mosaic virus protein 1a in RNA replication complex assembly and function. PLoS Pathog 5:e1000351

    PubMed Central  PubMed  Google Scholar 

  • Mandal D, Woolf TB, Rao R (2000) Manganese selectivity of pmr1, the yeast secretory pathway ion pump, is defined by residue gln783 in transmembrane segment 6. Residue Asp778 is essential for cation transport. J Biol Chem 275:23933–23938

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matsuda D, Dreher TW (2004) The tRNA-like structure of Turnip yellow mosaic virus RNA is a 3′-translational enhancer. Virology 321:36–46

    CAS  PubMed  Google Scholar 

  • Matsuda D, Yoshinari S, Dreher TW (2004) eEF1A binding to aminoacylated viral RNA represses minus strand synthesis by TYMV RNA-dependent RNA polymerase. Virology 321:47–56

    CAS  PubMed  Google Scholar 

  • Matto M, Sklan EH, David N, Melamed-Book N, Casanova JE, Glenn JS, Aroeti B (2011) Role for ADP ribosylation factor 1 in the regulation of hepatitis C virus replication. J Virol 85:946–956

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Memon AR (2004) The role of ADP-ribosylation factor and SAR1 in vesicular trafficking in plants. Biochim Biophys Acta 1664:9–30

    CAS  PubMed  Google Scholar 

  • Miller S, Krijnse-Locker J (2008) Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6:363–374

    CAS  PubMed  Google Scholar 

  • Mine A, Okuno T (2012) Composition of plant virus RNA replicase complexes. Curr Opin Virol 2:669–675

    CAS  PubMed  Google Scholar 

  • Mine A, Hyodo K, Takeda A, Kaido M, Mise K, Okuno T (2010a) 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

    CAS  PubMed  Google Scholar 

  • Mine A, Takeda A, Taniguchi T, Taniguchi H, Kaido M, Mise K, Okuno T (2010b) 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mine A, Hyodo K, Tajima Y, Kusumanegara K, Taniguchi T, Kaido M, Mise K, Taniguchi H, Okuno T (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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagy PD, Pogany J (2012) The dependence of viral RNA replication on co-opted host factors. Nat Rev Microbiol 10:137–149

    CAS  Google Scholar 

  • Nagy PD, Wang RY, Pogany J, Hafren A, Makinen K (2011) Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411:374–382

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishikiori M, Mori M, Dohi K, Okamura H, Katoh E, Naito S, Meshi T, Ishikawa M (2011) A host small GTP-binding protein ARL8 plays crucial roles in tobamovirus RNA replication. PLoS Pathog 7:e1002409

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishikiori M, Sugiyama S, Xiang H, Niiyama M, Ishibashi K, Inoue T, Ishikawa M, Matsumura H, Katoh E (2012) Crystal structure of the superfamily 1 helicase from Tomato mosaic virus. J Virol 86:7565–7576

    CAS  PubMed Central  PubMed  Google Scholar 

  • Noueiry AO, Diez J, Falk SP, Chen J, Ahlquist P (2003) Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol Cell Biol 23:4094–4106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nziengui H, Schoefs B (2009) Functions of reticulons in plants: what we can learn from animals and yeasts. Cell Mol Life Sci 66:584–595

    CAS  PubMed  Google Scholar 

  • Osman TA, Buck KW (1997) The tobacco mosaic virus RNA polymerase complex contains a plant protein related to the RNA-binding subunit of yeast eIF-3. J Virol 71:6075–6082

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25:635–646

    CAS  PubMed  Google Scholar 

  • Pathak KB, Sasvari Z, Nagy PD (2008) The host Pex19p plays a role in peroxisomal localization of tombusvirus replication proteins. Virology 379:294–305

    CAS  PubMed  Google Scholar 

  • Pogany J, Fabian MR, White KA, Nagy PD (2003) A replication silencer element in a plus-strand RNA virus. EMBO J 22:5602–5611

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pogany J, White KA, Nagy PD (2005) Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J Virol 79:4859–4869

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Prasanth KR, Huang YW, Liou MR, Wang RY, Hu CC, Tsai CH, Meng M, Lin NS, Hsu YH (2011) Glyceraldehyde 3-phosphate dehydrogenase negatively regulates the replication of Bamboo mosaic virus and its associated satellite RNA. J Virol 85:8829–8840

    CAS  PubMed Central  PubMed  Google Scholar 

  • Quadt R, Kao CC, Browning KS, Hershberger RP, Ahlquist P (1993) Characterization of a host protein associated with brome mosaic virus RNA-dependent RNA polymerase. Proc Natl Acad Sci USA 90:1498–1502

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rajendran KS, Nagy PD (2006) Kinetics and functional studies on interaction between the replicase proteins of Tomato Bushy Stunt Virus: requirement of p33:p92 interaction for replicase assembly. Virology 345:270–279

    CAS  PubMed  Google Scholar 

  • Reichel C, Beachy RN (1998) Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc Natl Acad Sci USA 95:11169–11174

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sasvari Z, Izotova L, Kinzy TG, Nagy PD (2011) Synergistic roles of eukaryotic translation elongation factors 1Bγ and 1A in stimulation of tombusvirus minus-strand synthesis. PLoS Pathog 7:e1002438

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sasvari Z, Kovalev N, Nagy PD (2013) The GEF1 proton-chloride exchanger affects tombusvirus replication via regulation of copper metabolism in yeast. J Virol 87:1800–1810

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schwartz M, Chen J, Janda M, Sullivan M, den Boon J, Ahlquist P (2002) A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell 9:505–514

    CAS  PubMed  Google Scholar 

  • Serva S, Nagy PD (2006) Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J Virol 80:2162–2169

    CAS  PubMed Central  PubMed  Google Scholar 

  • Serviene E, Shapka N, Cheng CP, Panavas T, Phuangrat B, Baker J, Nagy PD (2005) Genome-wide screen identifies host genes affecting viral RNA recombination. Proc Natl Acad Sci USA 102:10545–10550

    CAS  PubMed Central  PubMed  Google Scholar 

  • Serviene E, Jiang Y, Cheng CP, Baker J, Nagy PD (2006) Screening of the yeast yTHC collection identifies essential host factors affecting tombusvirus RNA recombination. J Virol 80:1231–1241

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shah Nawaz-ul-Rehman M, Martinez-Ochoa N, Pascal H, Sasvari Z, Herbst C, Xu K, Baker J, Sharma M, Herbst A, Nagy PD (2012) Proteome-wide overexpression of host proteins for identification of factors affecting tombusvirus RNA replication: an inhibitory role of protein kinase C. J Virol 86:9384–9395

    PubMed Central  PubMed  Google Scholar 

  • Shapka N, Stork J, Nagy PD (2005) Phosphorylation of the p33 replication protein of Cucumber necrosis tombusvirus adjacent to the RNA binding site affects viral RNA replication. Virology 343:65–78

    CAS  PubMed  Google Scholar 

  • Sharma M, Sasvari Z, Nagy PD (2010) Inhibition of sterol biosynthesis reduces tombusvirus replication in yeast and plants. J Virol 84:2270–2281

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sharma M, Sasvari Z, Nagy PD (2011) Inhibition of phospholipid biosynthesis decreases the activity of the tombusvirus replicase and alters the subcellular localization of replication proteins. Virology 415:141–152

    CAS  PubMed Central  PubMed  Google Scholar 

  • Simon AE, Miller WA (2013) 3′ Cap-independent translation enhancers of plant viruses. Annu Rev Microbiol 67:21–42

    CAS  PubMed  Google Scholar 

  • Stork J, Panaviene Z, Nagy PD (2005) Inhibition of in vitro RNA binding and replicase activity by phosphorylation of the p33 replication protein of Cucumber necrosis tombusvirus. Virology 343:79–92

    CAS  PubMed  Google Scholar 

  • Sun JH, Adkins S, Faurote G, Kao CC (1996) Initiation of (−)-strand RNA synthesis catalyzed by the BMV RNA-dependent RNA polymerase: synthesis of oligonucleotides. Virology 226:1–12

    CAS  PubMed  Google Scholar 

  • Tajima Y, Iwakawa HO, Kaido M, Mise K, Okuno T (2011) A long-distance RNA–RNA interaction plays an important role in programmed −1 ribosomal frameshifting in the translation of p88 replicase protein of Red clover necrotic mosaic virus. Virology 417:169–178

    CAS  PubMed  Google Scholar 

  • Taylor DN, Carr JP (2000) The GCD10 subunit of yeast eIF-3 binds the methyltransferase-like domain of the 126 and 183 kDa replicase proteins of tobacco mosaic virus in the yeast two-hybrid system. J Gen Virol 81:1587–1591

    CAS  PubMed  Google Scholar 

  • Theodoulou FL, Bernhardt K, Linka N, Baker A (2013) Peroxisome membrane proteins: multiple trafficking routes and multiple functions? Biochem J 451:345–352

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Tomita Y, Mizuno T, Díez J, Naito S, Ahlquist P, Ishikawa M (2003) Mutation of host DnaJ homolog inhibits brome mosaic virus negative-strand RNA synthesis. J Virol 77:2990–2997

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsujimoto Y, Numaga T, Ohshima K, Yano MA, Ohsawa R, Goto DB, Naito S, Ishikawa M (2003) Arabidopsis TOBAMOVIRUS MULTIPLICATION (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO J 22:335–343

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • van Dijk AA, Makeyev EV, Bamford DH (2004) Initiation of viral RNA-dependent RNA polymerization. J Gen Virol 85:1077–1093

    PubMed  Google Scholar 

  • Verchot J (2012) Cellular chaperones and folding enzymes are vital contributors to membrane bound replication and movement complexes during plant RNA virus infection. Front Plant Sci 3:275

    PubMed Central  PubMed  Google Scholar 

  • Verheije MH, Raaben M, Mari M, te Lintelo EG, Reggiori F, van Kuppeveld FJ, Rottier PJ, de Haan CA (2008) Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog 4:e1000088

    PubMed Central  PubMed  Google Scholar 

  • Wang X, Ahlquist P (2008) Brome mosaic virus (Bromoviridae). In: Mahy BWJ, van Regenmortel MHV (eds) Encyclopedia of virology, 3rd edn. Academic Press, New York, pp 381–386

    Google Scholar 

  • Wang RY, Nagy PD (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

    CAS  PubMed  Google Scholar 

  • Wang RY, Stork J, Nagy PD (2009) A key role for heat shock protein 70 in the localization and insertion of tombusvirus replication proteins to intracellular membranes. J Virol 83:3276–3287

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang X, Diaz A, Hao L, Gancarz B, den Boon JA, Ahlquist P (2011) Intersection of the multivesicular body pathway and lipid homeostasis in RNA replication by a positive-strand RNA virus. J Virol 85:5494–5503

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wei T, Wang A (2008) Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J Virol 82:12252–12264

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wei T, Zhang C, Hou X, Sanfaçon H, Wang A (2013) The SNARE protein Syp71 is essential for turnip mosaic virus infection by mediating fusion of virus-induced vesicles with chloroplasts. PLoS Pathog 9:e1003378

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong R, Wang A (2013) SCE1, the SUMO-conjugating enzyme in plants that interacts with NIb, the RNA-dependent RNA polymerase of Turnip mosaic virus, is required for viral infection. J Virol 87:4704–4715

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaji Y, Kobayashi T, Hamada K, Sakurai K, Yoshii A, Suzuki M, Namba S, Hibi T (2006) In vivo interaction between Tobacco mosaic virus RNA-dependent RNA polymerase and host translation elongation factor 1A. Virology 347:100–108

    CAS  PubMed  Google Scholar 

  • Yamaji Y, Sakurai K, Hamada K, Komatsu K, Ozeki J, Yoshida A, Yoshii A, Shimizu T, Namba S, Hibi T (2010) Significance of eukaryotic translation elongation factor 1A in tobacco mosaic virus infection. Arch Virol 155:263–268

    CAS  PubMed  Google Scholar 

  • Yamanaka T, Ohta T, Takahashi M, 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamanaka T, Imai T, Satoh R, Kawashima A, Takahashi M, Tomita K, Kubota K, Meshi T, Naito S, Ishikawa M (2002) Complete inhibition of tobamovirus multiplication by simultaneous mutations in two homologous host genes. J Virol 76:2491–2497

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zeenko VV, Ryabova LA, Spirin AS, Rothnie HM, Hess D, Browning KS, Hohn T (2002) Eukaryotic elongation factor 1A interacts with the upstream pseudoknot domain in the 3′ untranslated region of tobacco mosaic virus RNA. J Virol 76:5678–5691

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang J, Diaz A, Mao L, Ahlquist P, Wang X (2012) Host acyl coenzyme A binding protein regulates replication complex assembly and activity of a positive-strand RNA virus. J Virol 86:5110–5121

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu J, Gopinath K, Murali A, Yi G, Hayward SD, Zhu H, Kao C (2007) RNA-binding proteins that inhibit RNA virus infection. Proc Natl Acad Sci USA 104:3129–3134

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors apologize to those colleagues whose research on the replication of (+) RNA plant viruses is not mentioned in this review because of space restrictions. This work was supported in part by a Grant-in Aid for Scientific Research from the Japan Society for the Promotion of Science (JSPS) and in part by a Grant-in-Aid for JSPS fellows.

Author information

Authors and Affiliations

  1. Laboratory of Plant Pathology, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan

    Kiwamu Hyodo & Tetsuro Okuno

Authors
  1. Kiwamu Hyodo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tetsuro Okuno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tetsuro Okuno.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hyodo, K., Okuno, T. Host factors used by positive-strand RNA plant viruses for genome replication. J Gen Plant Pathol 80, 123–135 (2014). https://doi.org/10.1007/s10327-014-0505-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10327-014-0505-7

Keywords

Search

Navigation