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Citrus tristeza virus co-opts glyceraldehyde 3-phosphate dehydrogenase for its infectious cycle by interacting with the viral-encoded protein p23

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Citrus tristeza virus co-opts glyceraldehyde 3-phosphate dehydrogenase for its infectious cycle by interacting with the viral-encoded protein p23

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dc.contributor.author Ruiz Ruiz, Susana es_ES
dc.contributor.author Spano, R. es_ES
dc.contributor.author Navarro, Luis es_ES
dc.contributor.author Moreno, Pedro es_ES
dc.contributor.author Peña, L. es_ES
dc.contributor.author FLORES PEDAUYE, RICARDO es_ES
dc.date.accessioned 2020-06-02T05:37:36Z
dc.date.available 2020-06-02T05:37:36Z
dc.date.issued 2018-11-03 es_ES
dc.identifier.issn 0167-4412 es_ES
dc.identifier.uri http://hdl.handle.net/10251/144826
dc.description.abstract [EN] Key messageCitrus tristeza virus encodes a unique protein, p23, with multiple functional roles that include co-option of the cytoplasmic glyceraldehyde 3-phosphate dehydrogenase to facilitate the viral infectious cycle.AbstractThe genome of citrus tristeza virus (CTV), genus Closterovirus family Closteroviridae, is a single-stranded (+) RNA potentially encoding at least 17 proteins. One (p23), an RNA-binding protein of 209 amino acids with a putative Zn-finger and some basic motifs, displays singular features: (i) it has no homologues in other closteroviruses, (ii) it accumulates mainly in the nucleolus and Cajal bodies, and in plasmodesmata, and (iii) it mediates asymmetric accumulation of CTV RNA strands, intracellular suppression of RNA silencing, induction of some CTV syndromes and enhancement of systemic infection when expressed as a transgene ectopically or in phloem-associated cells in several Citrus spp. Here, a yeast two-hybrid screening of an expression library of Nicotiana benthamiana (a symptomatic experimental host for CTV), identified a transducin/WD40 domain protein and the cytosolic glyceraldehyde 3-phosphate dehydrogenase (GAPDH) as potential host interactors with p23. Bimolecular fluorescence complementation corroborated the p23-GAPDH interaction in planta and showed that p23 interacts with itself in the nucleolus, Cajal bodies and plasmodesmata, and with GAPDH in the cytoplasm (forming aggregates) and in plasmodesmata. The latter interaction was preserved in a p23 deletion mutant affecting the C-terminal domain, but not in two others affecting the Zn-finger and one internal basic motif. Virus-induced gene silencing of GAPDH mRNA resulted in a decrease of CTV titer as revealed by real-time RT-quantitative PCR and RNA gel-blot hybridization. Thus, like other viruses, CTV seems to co-opt GAPDH, via interaction with p23, to facilitate its infectious cycle. es_ES
dc.description.sponsorship This research was supported by a Grant (Prometeo/2008/121) from the Generalitat Valenciana, Spain, and by a Grant (AGL2009-08052) from the Ministerio de Ciencia e Innovación-Fondo Europeo de Desarrollo Regional. S. Ruiz-Ruiz has been additionally supported by a postdoctoral contract from the Generalitat Valenciana (APOSTD/2012/020, Program VALi+d). es_ES
dc.language Inglés es_ES
dc.publisher Springer-Verlag es_ES
dc.relation.ispartof Plant Molecular Biology es_ES
dc.rights Reserva de todos los derechos es_ES
dc.subject Citrus tristeza virus es_ES
dc.subject Closteroviruses es_ES
dc.subject Plant RNA viruses es_ES
dc.subject Virus-host interactions es_ES
dc.subject.classification BIOQUIMICA Y BIOLOGIA MOLECULAR es_ES
dc.title Citrus tristeza virus co-opts glyceraldehyde 3-phosphate dehydrogenase for its infectious cycle by interacting with the viral-encoded protein p23 es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1007/s11103-018-0783-0 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/Generalitat Valenciana//PROMETEO08%2F2008%2F121/ES/Biotecnología de cítricos/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//AGL2009-08052/ES/Mejora Genetica De La Calidad Y De La Respuesta A Estreses Bioticos De Los Citricos Mediante Ingenieria Genetica/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GV//APOSTD/2012/020/ es_ES
dc.rights.accessRights Cerrado es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia es_ES
dc.description.bibliographicCitation Ruiz Ruiz, S.; Spano, R.; Navarro, L.; Moreno, P.; Peña, L.; Flores Pedauye, R. (2018). Citrus tristeza virus co-opts glyceraldehyde 3-phosphate dehydrogenase for its infectious cycle by interacting with the viral-encoded protein p23. Plant Molecular Biology. 98(4-5):363-373. https://doi.org/10.1007/s11103-018-0783-0 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1007/s11103-018-0783-0 es_ES
dc.description.upvformatpinicio 363 es_ES
dc.description.upvformatpfin 373 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 98 es_ES
dc.description.issue 4-5 es_ES
dc.identifier.pmid 30392159 es_ES
dc.identifier.pmcid PMC7088584 es_ES
dc.relation.pasarela S\382549 es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder European Regional Development Fund es_ES
dc.contributor.funder Ministerio de Ciencia e Innovación es_ES
dc.description.references Albiach-Martí MR, Mawassi M, Gowda S, Satanarayana T, Hilf ME, Shanker S, Almira EC, Vives MC, López C, Guerri J, Flores R, Moren P, Garnsey SM, Dawson WO (2000) Sequences of citrus tristeza virus separated in time and space are essentially identical. J Virol 74:6856–6865 es_ES
dc.description.references Ambrós S, El-Mohtar C, Ruiz-Ruiz S, Peña L, Guerri J, Dawson WO, Moren P (2011) Agroinoculation of Citrus tristeza virus causes systemic infection and symptoms in the presumed nonhost Nicotiana benthamiana. Mol Plant Microb Interact 24:1119–1131 es_ES
dc.description.references Bar-Joseph M, Marcus R, Lee RF (1989) The continuous challenge of citrus tristeza virus control. Annu Rev Phytopathol 27:291–316 es_ES
dc.description.references Bartel PL, Chien C-T, Sternglanz R, Fields S (1993) Using the two-hybrid system to detect protein-protein interactions. In: Hartley DA (ed) Cellular interactions in development: a practical approach. Oxford University Press, Oxford, pp 153–179 es_ES
dc.description.references Bewick V, Cheek L, Ball J (2004) Statistics review 9: one-way analysis of variance. Crit Care 8:130–136 es_ES
dc.description.references Chambers TJ, Hahn CS, Galler R, Rice CM (1990) Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44:649–688 es_ES
dc.description.references Comellas M (2009) Estudio de la interacción entre naranjo amargo y el virus de la tristeza de los cítricos. Tesis doctoral. Universidad Politécnica de Valencia, Valencia es_ES
dc.description.references den Boon JA, Ahlquist P (2010) Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 64:241–256 es_ES
dc.description.references Dinesh-Kumar SP, Anandalakshmi R, Marathe R, Schiff M, Liu Y (2003) Virus-induced gene silencing. Methods Mol Biol 236:287–294 es_ES
dc.description.references Dollenmaier G, Weitz M (2003) Interaction of glyceraldehyde-3-phosphate dehydrogenase with secondary and tertiary RNA structural elements of the hepatitis A virus 3′ translated and non-translated regions. J Gen Virol 84:403–414 es_ES
dc.description.references Fagoaga C, López C, Moreno P, Navarro L, Flores R, Peña L (2005) Viral-like symptoms induced by the ectopic expression of the p23 of Citrus tristeza virus are citrus specific and do not correlate with the pathogenicity of the virus strain. Mol Plant-Microb Interact 18:435–445 es_ES
dc.description.references Fagoaga C, Pensabene G, Moreno P, Navarro L, Flores R, Peña L (2011) Ectopic expression of the p23 silencing suppressor of Citrus tristeza virus differentially modifies viral accumulation and tropism in two transgenic woody hosts. Mol Plant Pathol 12:898–910 es_ES
dc.description.references Flores R, Ruiz-Ruiz S, Soler N, Sánchez-Navarro J, Fagoaga C, López C, Navarro L, Moreno P, Peña L (2013) Citrus tristeza virus p23: a unique protein mediating key virus–host interactions. Front Microbiol 4:98 es_ES
dc.description.references French R, Ahlquist P (1987) Intercistronic as well as terminal sequences are required for efficient amplification of brome mosaic virus RNA3. J Virol 61:1457–1465 es_ES
dc.description.references Fromont-Racine M, Rain JC, Legrain P (1997) Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet 16:277–282 es_ES
dc.description.references García JA, Pallás V (2015) Viral factors involved in plant pathogenesis. Curr Opin Virol 11:21–30 es_ES
dc.description.references Ghorbel R, López C, Fagoaga C, Moreno P, Navarro L, Flores R, Peña L (2001) Transgenic citrus plants expressing the Citrus tristeza virus p23 protein exhibit viral-like symptoms. Mol Plant Pathol 2:27–36 es_ES
dc.description.references Gowda S, Satyanarayana T, Davis CL, Navas-Castillo J, Albiach-Martí MR, Mawassi M, Valkov N, Bar-Joseph M, Moreno P, Dawson WO (2000) The p20 gene product of Citrus tristeza virus accumulates in the amorphous inclusion bodies. Virology 274:246–254 es_ES
dc.description.references Harper SJ (2013) Citrus tristeza virus: evolution of complex and varied genotypic groups. Front Microbiol 4:93 es_ES
dc.description.references Heinlein M (2015) Plant virus replication and movement. Virology 479–480:657–671 es_ES
dc.description.references Hilf ME, Karasev AV, Pappu HR, Gumpf DJ, Niblett CL, Garnsey SM (1995) Characterization of citrus tristeza virus subgenomic RNAs in infected tissue. Virology 208:576–582 es_ES
dc.description.references 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 es_ES
dc.description.references Jenkins JL, Tanner JJ (2006) High-resolution structure of human D-glyceraldehyde-3-phosphate dehydrogenase. Acta Crystallogr D Biol Crystallogr 62:290–301 es_ES
dc.description.references Kaido M, Abe K, Mine A, Hyodo K, Taniguchi T, Taniguchi H, Mise K, Okuno T (2014) GAPDH-A recruits a plant virus movement protein to cortical virus replication complexes to facilitate viral cell-to-cell movement. PLoS Pathog 10:e1004505 es_ES
dc.description.references Kang SH, Dao TNM, Kim OK, Folimonova SY (2017) Self-interaction of Citrus tristeza virus p33 protein via N-terminal helix. Virus Res 233:29–34 es_ES
dc.description.references Karasev AV, Boyko VP, Gowda S, Nikolaeva O, Hilf ME, Koonin EV, Niblett CL, Cline K, Gumpf DJ, Lee RF, Garnsey SM, Lewandowski DJ, Dawson WO (1995) Complete sequence of the Citrus tristeza virus RNA genome. Virology 208:511–520 es_ES
dc.description.references Lai MMC, Cavanagh D (1997) The molecular biology of coronaviruses. Adv Virus Res 48:1–100 es_ES
dc.description.references López C, Navas-Castillo J, Gowda S, Moreno P, Flores R (2000) The 23 kDa protein coded by the 3′-terminal gene of Citrus tristeza virus is an RNA-binding protein. Virology 269:462–470 es_ES
dc.description.references Lu R, Folimonov A, Shintaku M, Li WX, Falk BW, Dawson WO, Ding SW (2004) Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc Natl Acad Sci USA 101:15742–15747 es_ES
dc.description.references Marsh LE, Huntley CC, Pogue GP, Connell JP, Hall TC (1991) Regulation of (+):(−) strand asymmetry in replication of brome mosaic virus RNA. Virology 182:76–83 es_ES
dc.description.references Mawassi M, Mietkiewska E, Gofman R, Yang G, Bar-Joseph M (1996) Unusual sequence relationships between two isolates of Citrus tristeza virus. J Gen Virol 77:2359–2364 es_ES
dc.description.references Moreno P, Ambrós S, Albiach-Martí MR, Guerri J, Peña L (2008) Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Mol Plant Pathol 9:251–268 es_ES
dc.description.references Nassuth A, Bol JF (1983) Altered balance of the synthesis of plus- and minus-strand RNAs induced by RNAs 1 and 2 of alfalfa mosaic virus in the absence of RNA3. Virology 124:75–85 es_ES
dc.description.references Petrik J, Parker H, Alexander G (1999) Human hepatic glyceraldehyde-3-phosphate dehydrogenase binds to the poly(U) tract of the 3′ non-coding region of hepatitis C virus genomic RNA. J Gen Virol 80:3109–3113 es_ES
dc.description.references Pogany J, Nagy PD (2008) Authentic replication and recombination of tomato bushy stunt virus RNA in a cell-free extract from yeast. J Virol 82:5967–5980 es_ES
dc.description.references 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 es_ES
dc.description.references Ruiz-Ruiz S, Moreno P, Guerri J, Ambrós S (2007) A real-time RT-PCR assay for detection and absolute quantitation of citrus tristeza virus in different plant tissues. J Virol Methods 145:96–105 es_ES
dc.description.references Ruiz-Ruiz S, Soler N, Sánchez-Navarro J, Fagoaga C, López C, Navarro L, Moreno P, Peña L, Flores R (2013) Citrus tristeza virus p23: determinants for nucleolar localization and their influence on suppression of RNA silencing and pathogenesis. Mol Plant Microb Interact 26:306–318 es_ES
dc.description.references Sambade A, López C, Rubio L, Flores R, Guerri J, Moreno P (2003) Polymorphism of a specific region in gene p23 of Citrus tristeza virus allows discrimination between mild and severe isolates. Arch Virol 148:2325–2340 es_ES
dc.description.references Satyanarayana T, Gowda S, Boyko VP, Albiach-Martí MR, Mawassi M, Navas-Castillo J, Karasev AV, Dolja V, Hilf ME, Lewandowski DJ, Moreno P, Bar-Joseph M, Garnsey SM, Dawson WO (1999) An engineered closterovirus RNA replicon and analysis of heterologous terminal sequences for replication. Proc Natl Acad Sci USA 96:7433–7438 es_ES
dc.description.references Satyanarayana T, Gowda S, Ayllón MA, Albiach-Martí MR, Rabindram R, Dawson WO (2002) The p23 protein of Citrus tristeza virus controls asymmetrical RNA accumulation. J Virol 76:473–483 es_ES
dc.description.references Soler N, Fagoaga C, López C, Moreno P, Navarro L, Flores R, Peña L (2014) Symptoms induced by transgenic expression of p23 from Citrus tristeza virus in phloem-associated cells of Mexican lime mimic virus infection without the aberrations accompanying constitutive expression. Mol Plant Pathol 16:388–399 es_ES
dc.description.references Vives MC, Rubio L, López C, Navas-Castillo J, Albiach-Martí MR, Dawson WO, Guerri J, Flores R, Moreno P (1999) The complete genome sequence of the major component of a mild Citrus tristeza virus isolate. J Gen Virol 80:811–816 es_ES
dc.description.references Vojtek AB, Hollenberg SM (1995) Ras-Raf interaction: two-hybrid analysis. Methods Enzymol 255:331–342 es_ES
dc.description.references Wang RY, Nagy PD (2008) Tomato bushy stunt virus coopts the RNA-binding function of a host metabolic enzyme for viral genomic RNA synthesis. Cell Host Microb 3:178–187 es_ES
dc.description.references White MR, Garcin ED (2016) The sweet side of RNA regulation: glyceraldehyde-3-phosphate dehydrogenase as a noncanonical RNA-binding protein. Wiley Interdisc Rev RNA 7:53–70 es_ES
dc.description.references Yang ZN, Mathews DH, Dodds JA, Mirkov TE (1999) Molecular characterization of an isolate of Citrus tristeza virus that causes severe symptoms in sweet orange. Virus Genes 19:131–142 es_ES
dc.description.references Yang SH, Liu M, Tien CF, Chou SJ, Chang RY (2009) Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) interaction with 3′ ends of Japanese encephalitis virus RNA and colocalization with the viral NS5 protein. J Biomed Sci 16:1–10 es_ES
dc.description.references Yi M, Schultz DE, Lemon SM (2000) Functional significance of the interaction of hepatitis A virus RNA with glyceraldehyde 3-phosphate dehydrogenase (GAPDH): opposing effects of GAPDH and polypyrimidine tract binding protein on internal ribosome entry site function. J Virol 74:6459–6468 es_ES


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