dc.contributor.author |
NAVARRO BOHIGUES, JOSE ANTONIO
|
es_ES |
dc.contributor.author |
Serra-Soriano, Marta
|
es_ES |
dc.contributor.author |
Corachán Valencia, Lorena
|
es_ES |
dc.contributor.author |
Pallás Benet, Vicente
|
es_ES |
dc.date.accessioned |
2021-11-05T12:37:03Z |
|
dc.date.available |
2021-11-05T12:37:03Z |
|
dc.date.issued |
2020-03-16 |
es_ES |
dc.identifier.issn |
2045-2322 |
es_ES |
dc.identifier.uri |
http://hdl.handle.net/10251/176118 |
|
dc.description.abstract |
[EN] Due to their minimal genomes, plant viruses are forced to hijack specific cellular pathways to ensure host colonization, a condition that most frequently involves physical interaction between viral and host proteins. Among putative viral interactors are the movement proteins, responsible for plasmodesma gating and genome binding during viral transport. Two of them, DGBp1 and DGBp2, are required for alpha-, beta- and gammacarmovirus cell-to-cell movement, but the number of DGBp-host interactors identified at present is limited. By using two different approaches, yeast two-hybrid and bimolecular fluorescence complementation assays, we found three Arabidopsis factors, eIF3g1, RPP3A and WRKY36, interacting with DGBp1s from each genus mentioned above. eIF3g1 and RPP3A are mainly involved in protein translation initiation and elongation phases, respectively, while WRKY36 belongs to WRKY transcription factor family, important regulators of many defence responses. These host proteins are not expected to be associated with viral movement, but knocking out WRKY36 or silencing either RPP3A or eIF3g1 negatively affected Arabidopsis infection by Turnip crinkle virus. A highly conserved FNF motif at DGBp1 C-terminus was required for protein-protein interaction and cell-to-cell movement, suggesting an important biological role. |
es_ES |
dc.description.sponsorship |
We thank Dr. Anne Simon and Dr. Steve A. Lommel for providing an infectious cDNA clone of the Turnip crinkle virus strain M (TCV-M) and PZP-TCV-sGFP plasmid, respectively. This work was funded by grant BIO2017-88321-R from the Spanish Agencia Estatal de Investigacion (AEI) and Fondo Europeo de Desarrollo Regional (FEDER). J.A.N. and M.S.-S. are the recipients of a postdoctoral contract and a PhD fellowship from the Ministerio de Ciencia, Innovacion y Universidades of Spain. |
es_ES |
dc.language |
Inglés |
es_ES |
dc.publisher |
Nature Publishing Group |
es_ES |
dc.relation.ispartof |
Scientific Reports |
es_ES |
dc.rights |
Reconocimiento (by) |
es_ES |
dc.title |
A conserved motif in three viral movement proteins from different genera is required for host factor recruitment and cell-to-cell movement |
es_ES |
dc.type |
Artículo |
es_ES |
dc.identifier.doi |
10.1038/s41598-020-61741-5 |
es_ES |
dc.relation.projectID |
info:eu-repo/grantAgreement/AEI//BIO2017-88321-R//DESCRIFRANDO INTERACCIONES VIRUS-PLANTA ESENCIALES PARA LA SUSCEPTIBILIDAD Y/O RESISTENCIA EN DOS PATOSISTEMAS AGRONOMICAMENTE RELEVANTES/ |
es_ES |
dc.rights.accessRights |
Abierto |
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.description.bibliographicCitation |
Navarro Bohigues, JA.; Serra-Soriano, M.; Corachán Valencia, L.; Pallás Benet, V. (2020). A conserved motif in three viral movement proteins from different genera is required for host factor recruitment and cell-to-cell movement. Scientific Reports. 10(1):1-15. https://doi.org/10.1038/s41598-020-61741-5 |
es_ES |
dc.description.accrualMethod |
S |
es_ES |
dc.relation.publisherversion |
https://doi.org/10.1038/s41598-020-61741-5 |
es_ES |
dc.description.upvformatpinicio |
1 |
es_ES |
dc.description.upvformatpfin |
15 |
es_ES |
dc.type.version |
info:eu-repo/semantics/publishedVersion |
es_ES |
dc.description.volume |
10 |
es_ES |
dc.description.issue |
1 |
es_ES |
dc.identifier.pmid |
32179855 |
es_ES |
dc.identifier.pmcid |
PMC7075923 |
es_ES |
dc.relation.pasarela |
S\433586 |
es_ES |
dc.contributor.funder |
Agencia Estatal de Investigación |
es_ES |
dc.contributor.funder |
European Regional Development Fund |
es_ES |
dc.contributor.funder |
Ministerio de Ciencia, Innovación y Universidades |
es_ES |
dc.description.references |
Sicard, A., Michalakis, Y., Gutiérrez, S. & Blanc, S. The strange lifestyle of multipartite viruses. PLoS Pathog. 12, e1005819–e1005819 (2016). |
es_ES |
dc.description.references |
Pita, J. S. & Roossinck, M. J. Virus populations, mutation rates and frequencies. In Plant Virus Evol. (ed. Roossinck, M. J.) 109–121 https://doi.org/10.1007/978-3-540-75763-4_6 (Springer Berlin Heidelberg, 2008). |
es_ES |
dc.description.references |
Ivanov, K. I. & Makinen, K. Coat proteins, host factors and plant viral replication. Curr. Opin. Virol. 2, 712–718 (2012). |
es_ES |
dc.description.references |
Wang, A. Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu. Rev. Phytopathol. 53, 45–66 (2015). |
es_ES |
dc.description.references |
García, J. A. & Pallás, V. Viral factors involved in plant pathogenesis. Curr. Opin. Virol. 10, 21–30 (2015). |
es_ES |
dc.description.references |
Garcia-Ruiz, H. Host factors against plant viruses. Mol. Plant Pathol. 20, 1588–1601 (2019). |
es_ES |
dc.description.references |
Hull, R. Induction of disease 1: virus movement through the plant and effects on plant metabolism. In Matthews’ Plant Virology (ed. Hull, R.) 373–436 (Academic Press, 2002). |
es_ES |
dc.description.references |
Navarro, J. A. & Pallas, V. An update on the intracellular and intercellular trafficking of carmoviruses. Front. Plant. Sci. 8, 1801 (2017). |
es_ES |
dc.description.references |
Azevedo, J. et al. Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev. 24, 904–915 (2010). |
es_ES |
dc.description.references |
Zhang, X., Zhang, X., Singh, J., Li, D. & Qu, F. Temperature-dependent survival of Turnip crinkle virus-infected arabidopsis plants relies on an RNA silencing-based defense that requires dcl2, AGO2, and HEN1. J. Virol. 86, 6847–6854 (2012). |
es_ES |
dc.description.references |
Donze, T., Qu, F., Twigg, P. & Morris, T. J. Turnip crinkle virus coat protein inhibits the basal immune response to virus invasion in Arabidopsis by binding to the NAC transcription factor TIP. Virology 449, 207–214 (2014). |
es_ES |
dc.description.references |
Lin, B. & Heaton, L. A. An Arabidopsis thaliana protein interacts with a movement protein of Turnip crinkle virus in yeast cells and in vitro. J. Gen. Virol. 82, 1245–1251 (2001). |
es_ES |
dc.description.references |
Navarro, J. A., Sanchez-Navarro, J. A. & Pallas, V. Key checkpoints in the movement of plant viruses through the host. Adv. Virus Res. 104, 1–64 (2019). |
es_ES |
dc.description.references |
Navarro, J. A. et al. RNA-binding properties and membrane insertion of Melon necrotic spot virus (MNSV) double gene block movement proteins. Virology 356, 57–67 (2006). |
es_ES |
dc.description.references |
Serra-Soriano, M., Pallás, V. & Navarro, J. A. A model for transport of a viral membrane protein through the early secretory pathway: minimal sequence and endoplasmic reticulum lateral mobility requirements. Plant J. 77, 863–879 (2014). |
es_ES |
dc.description.references |
Genoves, A., Navarro, J. A. & Pallas, V. Functional analysis of the five melon necrotic spot virus genome-encoded proteins. J. Gen. Virol. 87, 2371–2380 (2006). |
es_ES |
dc.description.references |
Li, W. Z., Qu, F. & Morris, T. J. Cell-to-cell movement of turnip crinkle virus is controlled by two small open reading frames that function in trans. Virology 244, 405–416 (1998). |
es_ES |
dc.description.references |
Martinez-Turino, S. & Hernandez, C. A membrane-associated movement protein of Pelargonium flower break virus shows RNA-binding activity and contains a biologically relevant leucine zipper-like motif. Virology 413, 310–319 (2011). |
es_ES |
dc.description.references |
Molnár, A., Havelda, Z., Dalmay, T., Szutorisz, H. & Burgyán, J. Complete nucleotide sequence of tobacco necrosis virus strain D(H) and genes required for RNA replication and virus movement. J. Gen. Virol. 78(6), 1235–1239 (1997). |
es_ES |
dc.description.references |
Marcos, J. F., Vilar, M., Pérez-Payá, E. & Pallás, V. In vivo detection, RNA-binding properties and characterization of the RNA-binding domain of the p7 putative movement protein from Carnation mottle carmovirus (CarMV). Virology 255, 354–365 (1999). |
es_ES |
dc.description.references |
Vilar, M., Esteve, V., Pallás, V., Marcos, J. F. & Pérez-Payá, E. Structural properties of carnation mottle virus p7 movement protein and its RNA-binding domain. J. Biol. Chem. 276, 18122–18129 (2001). |
es_ES |
dc.description.references |
Vilar, M., Saurí, A., Marcos, J. F., Mingarro, I. & Pérez‐Payá, E. Transient structural ordering of the RNA‐binding domain of carnation mottle virus p7 movement protein modulates nucleic acid binding. Chembiochem 6, 1391–1396 (2005). |
es_ES |
dc.description.references |
Genoves, A., Navarro, J. A. & Pallas, V. A self-interacting carmovirus movement protein plays a role in binding of viral RNA during the cell-to-cell movement and shows an actin cytoskeleton dependent location in cell periphery. Virology 395, 133–142 (2009). |
es_ES |
dc.description.references |
Garcia-Castillo, S., Sanchez-Pina, M. A. & Pallas, V. Spatio-temporal analysis of the RNAs, coat and movement (p7) proteins of Carnation mottle virus in Chenopodium quinoa plants. J. Gen. Virol. 84, 745–749 (2003). |
es_ES |
dc.description.references |
Cohen, Y., Qu, F., Gisel, A., Morris, T. J. & Zambryski, P. C. Nuclear localization of turnip crinkle virus movement protein p8. Virology 273, 276–285 (2000). |
es_ES |
dc.description.references |
Martinez-Gil, L., Sauri, A., Vilar, M., Pallas, V. & Mingarro, I. Membrane insertion and topology of the p7B movement protein of Melon Necrotic Spot Virus (MNSV). Virology 367, 348–357 (2007). |
es_ES |
dc.description.references |
Sauri, A., Saksena, S., Salgado, J., Johnson, A. E. & Mingarro, I. Double-spanning plant viral movement protein integration into the endoplasmic reticulum membrane is signal recognition particle-dependent, translocon-mediated, and concerted. J. Biol. Chem. 280, 25907–25912 (2005). |
es_ES |
dc.description.references |
Genoves, A., Navarro, J. A. & Pallas, V. The intra- and intercellular movement of Melon necrotic spot virus (MNSV) depends on an active secretory pathway. Mol. Plant-Microbe Interact. 23, 263–272 (2010). |
es_ES |
dc.description.references |
Aparicio, F. & Pallás, V. The coat protein of Alfalfa mosaic virus interacts and interferes with the transcriptional activity of the bHLH transcription factor ILR3 promoting salicylic acid-dependent defence signalling response. Mol. Plant Pathol. 18(2), 173–186 (2017). |
es_ES |
dc.description.references |
Yang, Y. et al. UVR8 interacts with WRKY36 to regulate HY5 transcription and hypocotyl elongation in Arabidopsis. Nat. Plants 4, 98–107 (2018). |
es_ES |
dc.description.references |
Cutler, S. R., Ehrhardt, D. W., Griffitts, J. S. & Somerville, C. R. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. USA 97, 3718–3723 (2000). |
es_ES |
dc.description.references |
La Cour, T. et al. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17, 527–536 (2004). |
es_ES |
dc.description.references |
Prieto, G., Fullaondo, A. & Rodriguez, J. A. Prediction of nuclear export signals using weighted regular expressions (Wregex). Bioinformatics 30, 1220–1227 (2014). |
es_ES |
dc.description.references |
Wobbe, K. K., Akgoz, M., Dempsey, D. A. & Klessig, D. F. A single amino acid change in turnip crinkle virus movement protein p8 affects RNA binding and virulence on Arabidopsis thaliana. J. Virol. 72, 6247–6250 (1998). |
es_ES |
dc.description.references |
Akgoz, M., Nguyen, Q. N., Talmadge, A. E., Drainville, K. E. & Wobbe, K. K. Mutational analysis of Turnip crinkle virus movement protein p8. Mol. Plant Pathol. 2(1), 37–48, https://doi.org/10.1046/j.1364-3703.2001.00048.x (2001). |
es_ES |
dc.description.references |
Ahlfors, R. et al. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16, 1925–1937 (2004). |
es_ES |
dc.description.references |
Aravind, L. The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem. Sci. 26, 273–275 (2001). |
es_ES |
dc.description.references |
Meyer, E. A., Castellano, R. K. & Diederich, F. Interactions with aromatic rings in chemical and biological recognition. Angew. Chem. Int. Ed. Engl. 42, 1210–1250 (2003). |
es_ES |
dc.description.references |
Profit, A. A., Felsen, V., Chinwong, J., Mojica, E. R. & Desamero, R. Z. Evidence of pi-stacking interactions in the self-assembly of hIAPP(22-29). Proteins 81, 690–703 (2013). |
es_ES |
dc.description.references |
Amari, K., Vazquez, F. & Heinlein, M. Manipulation of plant host susceptibility: an emerging role for viral movement proteins? Front. Plant. Sci. 3, 10 (2012). |
es_ES |
dc.description.references |
Morozov, S. Y. & Solovyev, A. G. Did silencing suppression counter-defensive strategy contribute to origin and evolution of the triple gene block coding for plant virus movement proteins? Front. Plant. Sci. 3, 136 (2012). |
es_ES |
dc.description.references |
Levy, A., Zheng, J. Y. & Lazarowitz, S. G. The tobamovirus turnip vein clearing virus 30-kilodalton movement protein localizes to novel nuclear filaments to enhance virus infection. J. Virol. 87, 6428–6440 (2013). |
es_ES |
dc.description.references |
Gonzalo, P. & Reboud, J. P. The puzzling lateral flexible stalk of the ribosome. Biol. Cell. 95, 179–193 (2003). |
es_ES |
dc.description.references |
Szick, K., Springer, M. & Bailey-Serres, J. Evolutionary analyses of the 12-kDa acidic ribosomal P-proteins reveal a distinct protein of higher plant ribosomes. Proc. Natl. Acad. Sci. USA 95, 2378–2383 (1998). |
es_ES |
dc.description.references |
Hafren, A., Eskelin, K. & Makinen, K. Ribosomal protein P0 promotes Potato virus A infection and functions in viral translation together with VPg and eIF(iso)4E. J. Virol. 87, 4302–4312 (2013). |
es_ES |
dc.description.references |
Sato, H. et al. Measles virus N protein inhibits host translation by binding to eIF3-p40. J. Virol. 81, 11569–11576 (2007). |
es_ES |
dc.description.references |
Bhardwaj, U., Powell, P. & Goss, D. J. Eukaryotic initiation factor (eIF) 3 mediates barley yellow dwarf viral mRNA 3′–5′ UTR interactions and 40S ribosomal subunit binding to facilitate cap-independent translation. Nucleic Acids Res. 47, 6225–6235 |
es_ES |
dc.description.references |
Park, H. S., Himmelbach, A., Browning, K. S., Hohn, T. & Ryabova, L. A. A plant viral ‘reinitiation’ factor interacts with the host translational machinery. Cell 106, 723–733 (2001). |
es_ES |
dc.description.references |
Thiébeauld, O., Pooggin, M. & Ryabova, L. Alternative translation strategies in plant viruses. Plant Viruses 1, 1–20 (2007). |
es_ES |
dc.description.references |
Bureau, M. et al. P6 protein of Cauliflower mosaic virus, a translation reinitiator, interacts with ribosomal protein L13 from Arabidopsis thaliana. J. Gen. Virol. 85, 3765–3775 (2004). |
es_ES |
dc.description.references |
Ryabova, L. A., Pooggin, M. M. & Hohn, T. Translation reinitiation and leaky scanning in plant viruses. Virus Res. 119, 52–62 (2006). |
es_ES |
dc.description.references |
Chen, L., Zhang, L., Li, D., Wang, F. & Yu, D. WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 110, E1963–E1971 (2013). |
es_ES |
dc.description.references |
Huh, S. U., Choi, L. M., Lee, G. J., Kim, Y. J. & Paek, K. H. Capsicum annuum WRKY transcription factor d (CaWRKYd) regulates hypersensitive response and defense response upon Tobacco mosaic virus infection. Plant Sci. 197, 50–58 (2012). |
es_ES |
dc.description.references |
Menke, F. L. et al. Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol. Plant Microbe Interact. 18, 1027–1034 (2005). |
es_ES |
dc.description.references |
Park, H. S. & Kim, K. H. Virus-induced silencing of the WRKY1 transcription factor that interacts with the SL1 structure of Potato virus X leads to higher viral RNA accumulation and severe necrotic symptoms. Plant Pathol. J. 28, 40–48 (2012). |
es_ES |
dc.description.references |
Gao, R., Liu, P., Yong, Y. & Wong, S. M. Genome-wide transcriptomic analysis reveals correlation between higher WRKY61 expression and reduced symptom severity in Turnip crinkle virus infected Arabidopsis thaliana. Sci. Rep. 6, 24604 (2016). |
es_ES |
dc.description.references |
Zou, L. et al. Transcription factor WRKY30 mediates resistance to Cucumber mosaic virus in Arabidopsis. Biochem. Biophys. Res. Commun. 517, 118–124 (2019). |
es_ES |
dc.description.references |
Huang, Y. et al. Members of WRKY Group III transcription factors are important in TYLCV defense signaling pathway in tomato (Solanum lycopersicum). BMC Genomics 17, 788 (2016). |
es_ES |
dc.description.references |
Besseau, S., Li, J. & Palva, E. T. WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 63, 2667–2679 (2012). |
es_ES |
dc.description.references |
Yan, L. et al. Auto- and cross-repression of three arabidopsis WRKY transcription factors WRKY18, WRKY40, and WRKY60 negatively involved in ABA signaling. J. Plant Growth Regul. 32, 399–416 (2013). |
es_ES |
dc.description.references |
Xu, E., Vaahtera, L. & Brosché, M. Roles of defense hormones in the regulation of ozone-induced changes in gene expression and cell death. Mol. Plant 8, 1776–1794 (2015). |
es_ES |
dc.description.references |
Li, S.-W., Leng, Y. & Shi, R.-F. Transcriptomic profiling provides molecular insights into hydrogen peroxide-induced adventitious rooting in mung bean seedlings. BMC Genomics 18, 188 (2017). |
es_ES |
dc.description.references |
Imran, Q. M. et al. Transcriptome wide identification and characterization of NO-responsive WRKY transcription factors in Arabidopsis thaliana L. Environ. Exp. Bot. 148, 128–143 (2018). |
es_ES |
dc.description.references |
Hernandez, J. et al. Oxidative stress and antioxidative responses in plant–virus interactions. Physiol. Mol. Plant Pathol. 94, 134–148 (2015). |
es_ES |
dc.description.references |
Ahlfors, R., Brosche, M., Kollist, H. & Kangasjarvi, J. Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J. 58, 1–12 (2009). |
es_ES |
dc.description.references |
Oh, J. W., Kong, Q., Song, C., Carpenter, C. D. & Simon, A. E. Open reading frames of Turnip crinkle virus involved in satellite symptom expression and incompatibility with Arabidopsis thaliana ecotype Dijon. Mol. Plant Microbe Interact. 8, 979–987 (1995). |
es_ES |
dc.description.references |
Gietz, R. D. & Woods, R. A. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzym. 350, 87–96 (2002). |
es_ES |
dc.description.references |
Nemeth, K. et al. Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev. 12, 3059–3073 (1998). |
es_ES |
dc.description.references |
Knoester, M. et al. Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc. Natl. Acad. Sci. USA 95, 1933–1937 (1998). |
es_ES |
dc.description.references |
Liu, Y., Schiff, M., Marathe, R. & Dinesh-Kumar, S. P. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30, 415–429 (2002). |
es_ES |
dc.description.references |
Fernandez-Pozo, N., Rosli, H. G., Martin, G. B. & Mueller, L. A. The SGN VIGS tool: user-friendly software to design virus-induced gene silencing (VIGS) constructs for functional genomics. Mol. Plant 8, 486–488 (2015). |
es_ES |
dc.description.references |
Martínez-Pérez, M. et al. Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proc. Natl. Acad. Sci. USA 114, 10755–10760 (2017). |
es_ES |
dc.description.references |
Powers, J. G. et al. A versatile assay for the identification of RNA silencing suppressors based on complementation of viral movement. Mol. Plant-Microbe Interact. 21(7), 879–890, https://doi.org/10.1094/MPMI-21-7-0879 (2008). |
es_ES |
dc.description.references |
Pallas, V., Mas, P. & Sanchez-Navarro, J. A. Detection of plant RNA viruses by nonisotopic dot-blot hybridization. Methods Mol. Biol. 81, 461–468 (1998). |
es_ES |
dc.description.references |
Navarro, J. A., Serra-Soriano, M. & Pallás, V. A Protocol to Measure the Extent of Cell-to-cell Movement of RNA Viruses in Planta. Bio-protocol 4, e1269 (2014). |
es_ES |
dc.description.references |
Koressaar, T. et al. Primer3_masker: integrating masking of template sequence with primer design software. Bioinformatics 34, 1937–1938 (2018). |
es_ES |
dc.description.references |
Lilly, S. T., Drummond, R. S., Pearson, M. N. & MacDiarmid, R. M. Identification and validation of reference genes for normalization of transcripts from virus-infected Arabidopsis thaliana. Mol. Plant Microbe Interact. 24, 294–304 (2011). |
es_ES |