Molecular signatures of silencing suppression degeneracy from a complex RNA virus

As genomic architectures become more complex, they begin to accumulate degenerate and redundant elements. However, analyses of the molecular mechanisms underlying these genetic architecture features remain scarce, especially in compact but sufficiently complex genomes. In the present study, we follo...

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Autores principales: Gómez-Munoz, Neus, Gimenez-Santamarina, Silvia, Sanchez-Vicente, Javier, Navarro-López, Josep, Martínez, Fernando, Daros, José A., Rodrigo, Guillermo
Formato: article
Lenguaje:Inglés
Publicado: PLOS 2021
Materias:
Acceso en línea:http://hdl.handle.net/20.500.11939/7565
https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1009166
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author Gómez-Munoz, Neus
Gimenez-Santamarina, Silvia
Sanchez-Vicente, Javier
Navarro-López, Josep
Martínez, Fernando
Daros, José A.
Rodrigo, Guillermo
author_browse Daros, José A.
Gimenez-Santamarina, Silvia
Gómez-Munoz, Neus
Martínez, Fernando
Navarro-López, Josep
Rodrigo, Guillermo
Sanchez-Vicente, Javier
author_facet Gómez-Munoz, Neus
Gimenez-Santamarina, Silvia
Sanchez-Vicente, Javier
Navarro-López, Josep
Martínez, Fernando
Daros, José A.
Rodrigo, Guillermo
author_sort Gómez-Munoz, Neus
collection ReDivia
description As genomic architectures become more complex, they begin to accumulate degenerate and redundant elements. However, analyses of the molecular mechanisms underlying these genetic architecture features remain scarce, especially in compact but sufficiently complex genomes. In the present study, we followed a proteomic approach together with a computational network analysis to reveal molecular signatures of protein function degeneracy from a plant virus (as virus-host protein-protein interactions). We employed affinity purification coupled to mass spectrometry to detect several host factors interacting with two proteins of Citrus tristeza virus (p20 and p25) that are known to function as RNA silencing suppressors, using an experimental system of transient expression in a model plant. The study was expanded by considering two different isolates of the virus, and some key interactions were confirmed by bimolecular fluorescence complementation assays. We found that p20 and p25 target a common set of plant proteins including chloroplastic proteins and translation factors. Moreover, we noted that even specific targets of each viral protein overlap in function. Notably, we identified argonaute proteins (key players in RNA silencing) as reliable targets of p20. Furthermore, we found that these viral proteins preferentially do not target hubs in the host protein interactome, but elements that can transfer information by bridging different parts of the interactome. Overall, our results demonstrate that two distinct proteins encoded in the same viral genome that overlap in function also overlap in their interactions with the cell proteome, thereby highlighting an overlooked connection from a degenerate viral system.
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spelling ReDivia75652025-04-25T14:48:23Z Molecular signatures of silencing suppression degeneracy from a complex RNA virus Gómez-Munoz, Neus Gimenez-Santamarina, Silvia Sanchez-Vicente, Javier Navarro-López, Josep Martínez, Fernando Daros, José A. Rodrigo, Guillermo RNA virus Molecular signatures RNA silencing supressors H20 Plant diseases U30 Research methods F30 Plant genetics and breeding Citrus tristeza virus Genomes Plant viruses Mass spectrometry As genomic architectures become more complex, they begin to accumulate degenerate and redundant elements. However, analyses of the molecular mechanisms underlying these genetic architecture features remain scarce, especially in compact but sufficiently complex genomes. In the present study, we followed a proteomic approach together with a computational network analysis to reveal molecular signatures of protein function degeneracy from a plant virus (as virus-host protein-protein interactions). We employed affinity purification coupled to mass spectrometry to detect several host factors interacting with two proteins of Citrus tristeza virus (p20 and p25) that are known to function as RNA silencing suppressors, using an experimental system of transient expression in a model plant. The study was expanded by considering two different isolates of the virus, and some key interactions were confirmed by bimolecular fluorescence complementation assays. We found that p20 and p25 target a common set of plant proteins including chloroplastic proteins and translation factors. Moreover, we noted that even specific targets of each viral protein overlap in function. Notably, we identified argonaute proteins (key players in RNA silencing) as reliable targets of p20. Furthermore, we found that these viral proteins preferentially do not target hubs in the host protein interactome, but elements that can transfer information by bridging different parts of the interactome. Overall, our results demonstrate that two distinct proteins encoded in the same viral genome that overlap in function also overlap in their interactions with the cell proteome, thereby highlighting an overlooked connection from a degenerate viral system. 2021-08-25T15:45:52Z 2021-08-25T15:45:52Z 2021 article publishedVersion Ambrós, S., Gómez-Muñoz, N., Giménez-Santamarina, S., Sánchez-Vicente, J., Navarro-López, J., Martínez, F. et al. (2021) Molecular signatures of silencing suppression degeneracy from a complex RNA virus. PLoS Comput Biol 17(6): e1009166. 1553-7358 1553-734X (e-ISSN) http://hdl.handle.net/20.500.11939/7565 10.1371/journal.pcbi.1009166 https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1009166 en info:eu-repo/grantAgreement/MICINN//AGL2010-20221/ES/BASES MOLECULARES PARA EL DIAGNOSTICO Y CONTROL DE LAS CEPAS VIRULENTAS DEL VIRUS DE LA TRISTEZA DE LOS CITRICOS (CTV)/ info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-83184-R/ES/VIRUS DE PLANTAS: PATOGENOS Y TAMBIEN VECTORES PARA LA PRODUCCION DE PROTEINAS, METABOLITOS, RNAS Y NANOPARTICULAS/ info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-101410-B-I00/ES/BIOLOGIA DE SISTEMAS DE RIBORREGULACION SINTETICA: TERMODINAMICA, RUIDO Y OPERABILIDAD/ This work was supported by the grants PROMETEO/2019/012 from the Valencian Regional Government (to SA), as well as grants AGL2010- 20221/AGR, BIO2017-83184-R, and PGC2018-101410-B-I00 from the Spanish Ministry of Science, Innovation, and Universities (to SA, JAD, and GR, respectively). The two latter grants were co-financed by the European Regional Development Fund. Atribución-NoComercial-SinDerivadas 3.0 España http://creativecommons.org/licenses/by-nc-nd/3.0/es/ openAccess PLOS electronico
spellingShingle RNA virus
Molecular signatures
RNA silencing supressors
H20 Plant diseases
U30 Research methods
F30 Plant genetics and breeding
Citrus tristeza virus
Genomes
Plant viruses
Mass spectrometry
Gómez-Munoz, Neus
Gimenez-Santamarina, Silvia
Sanchez-Vicente, Javier
Navarro-López, Josep
Martínez, Fernando
Daros, José A.
Rodrigo, Guillermo
Molecular signatures of silencing suppression degeneracy from a complex RNA virus
title Molecular signatures of silencing suppression degeneracy from a complex RNA virus
title_full Molecular signatures of silencing suppression degeneracy from a complex RNA virus
title_fullStr Molecular signatures of silencing suppression degeneracy from a complex RNA virus
title_full_unstemmed Molecular signatures of silencing suppression degeneracy from a complex RNA virus
title_short Molecular signatures of silencing suppression degeneracy from a complex RNA virus
title_sort molecular signatures of silencing suppression degeneracy from a complex rna virus
topic RNA virus
Molecular signatures
RNA silencing supressors
H20 Plant diseases
U30 Research methods
F30 Plant genetics and breeding
Citrus tristeza virus
Genomes
Plant viruses
Mass spectrometry
url http://hdl.handle.net/20.500.11939/7565
https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1009166
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