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A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes

Viruses are obligate intracellular parasites that have co-evolved with their hosts to establish an intricate network of protein–protein interactions. Here, we followed a high-throughput yeast two-hybrid screening to identify 378 novel protein–protein interactions between turnip mosaic virus (TuMV) a...

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Autores principales: Martínez, Fernando, Carrasco, José L., Toft, Christina, Hillung, Julia, Giménez-Santamarina, Silvia, Yenush, Lynne, Rodrigo, Guillermo, Elena, Santiago F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9834402/
https://www.ncbi.nlm.nih.gov/pubmed/36631662
http://dx.doi.org/10.1038/s42003-023-04427-8
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author Martínez, Fernando
Carrasco, José L.
Toft, Christina
Hillung, Julia
Giménez-Santamarina, Silvia
Yenush, Lynne
Rodrigo, Guillermo
Elena, Santiago F.
author_facet Martínez, Fernando
Carrasco, José L.
Toft, Christina
Hillung, Julia
Giménez-Santamarina, Silvia
Yenush, Lynne
Rodrigo, Guillermo
Elena, Santiago F.
author_sort Martínez, Fernando
collection PubMed
description Viruses are obligate intracellular parasites that have co-evolved with their hosts to establish an intricate network of protein–protein interactions. Here, we followed a high-throughput yeast two-hybrid screening to identify 378 novel protein–protein interactions between turnip mosaic virus (TuMV) and its natural host Arabidopsis thaliana. We identified the RNA-dependent RNA polymerase NIb as the viral protein with the largest number of contacts, including key salicylic acid-dependent transcription regulators. We verified a subset of 25 interactions in planta by bimolecular fluorescence complementation assays. We then constructed and analyzed a network comprising 399 TuMV-A. thaliana interactions together with intravirus and intrahost connections. In particular, we found that the host proteins targeted by TuMV are enriched in different aspects of plant responses to infections, are more connected and have an increased capacity to spread information throughout the cell proteome, display higher expression levels, and have been subject to stronger purifying selection than expected by chance. The proviral or antiviral role of ten host proteins was validated by characterizing the infection dynamics in the corresponding mutant plants, supporting a proviral role for the transcriptional regulator TGA1. Comparison with similar studies with animal viruses, highlights shared fundamental features in their mode of action.
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spelling pubmed-98344022023-01-13 A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes Martínez, Fernando Carrasco, José L. Toft, Christina Hillung, Julia Giménez-Santamarina, Silvia Yenush, Lynne Rodrigo, Guillermo Elena, Santiago F. Commun Biol Article Viruses are obligate intracellular parasites that have co-evolved with their hosts to establish an intricate network of protein–protein interactions. Here, we followed a high-throughput yeast two-hybrid screening to identify 378 novel protein–protein interactions between turnip mosaic virus (TuMV) and its natural host Arabidopsis thaliana. We identified the RNA-dependent RNA polymerase NIb as the viral protein with the largest number of contacts, including key salicylic acid-dependent transcription regulators. We verified a subset of 25 interactions in planta by bimolecular fluorescence complementation assays. We then constructed and analyzed a network comprising 399 TuMV-A. thaliana interactions together with intravirus and intrahost connections. In particular, we found that the host proteins targeted by TuMV are enriched in different aspects of plant responses to infections, are more connected and have an increased capacity to spread information throughout the cell proteome, display higher expression levels, and have been subject to stronger purifying selection than expected by chance. The proviral or antiviral role of ten host proteins was validated by characterizing the infection dynamics in the corresponding mutant plants, supporting a proviral role for the transcriptional regulator TGA1. Comparison with similar studies with animal viruses, highlights shared fundamental features in their mode of action. Nature Publishing Group UK 2023-01-11 /pmc/articles/PMC9834402/ /pubmed/36631662 http://dx.doi.org/10.1038/s42003-023-04427-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Martínez, Fernando
Carrasco, José L.
Toft, Christina
Hillung, Julia
Giménez-Santamarina, Silvia
Yenush, Lynne
Rodrigo, Guillermo
Elena, Santiago F.
A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes
title A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes
title_full A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes
title_fullStr A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes
title_full_unstemmed A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes
title_short A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes
title_sort binary interaction map between turnip mosaic virus and arabidopsis thaliana proteomes
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9834402/
https://www.ncbi.nlm.nih.gov/pubmed/36631662
http://dx.doi.org/10.1038/s42003-023-04427-8
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