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RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants

Many plant viruses express suppressor proteins (VSRs) that can inhibit RNA silencing, a central component of antiviral plant immunity. The most common activity of VSRs is the high-affinity binding of virus-derived siRNAs and thus their sequestration from the silencing process. Since siRNAs share lar...

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Autores principales: Pertermann, Robert, Golbik, Ralph Peter, Tamilarasan, Selvaraj, Gursinsky, Torsten, Gago-Zachert, Selma, Pantaleo, Vitantonio, Thondorf, Iris, Behrens, Sven-Erik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9103804/
https://www.ncbi.nlm.nih.gov/pubmed/35563369
http://dx.doi.org/10.3390/ijms23094977
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author Pertermann, Robert
Golbik, Ralph Peter
Tamilarasan, Selvaraj
Gursinsky, Torsten
Gago-Zachert, Selma
Pantaleo, Vitantonio
Thondorf, Iris
Behrens, Sven-Erik
author_facet Pertermann, Robert
Golbik, Ralph Peter
Tamilarasan, Selvaraj
Gursinsky, Torsten
Gago-Zachert, Selma
Pantaleo, Vitantonio
Thondorf, Iris
Behrens, Sven-Erik
author_sort Pertermann, Robert
collection PubMed
description Many plant viruses express suppressor proteins (VSRs) that can inhibit RNA silencing, a central component of antiviral plant immunity. The most common activity of VSRs is the high-affinity binding of virus-derived siRNAs and thus their sequestration from the silencing process. Since siRNAs share large homologies with miRNAs, VSRs like the Tombusvirus p19 may also bind miRNAs and in this way modulate cellular gene expression at the post-transcriptional level. Interestingly, the binding affinity of p19 varies considerably between different miRNAs, and the molecular determinants affecting this property have not yet been adequately characterized. Addressing this, we analyzed the binding of p19 to the miRNAs 162 and 168, which regulate the expression of the important RNA silencing constituents Dicer-like 1 (DCL1) and Argonaute 1 (AGO1), respectively. p19 binds miRNA162 with similar high affinity as siRNA, whereas the affinity for miRNA168 is significantly lower. We show that specific molecular features, such as mismatches and ‘G–U wobbles’ on the RNA side and defined amino acid residues on the VSR side, mediate this property. Our observations highlight the remarkable adaptation of VSR binding affinities to achieve differential effects on host miRNA activities. Moreover, they show that even minimal changes, i.e., a single base pair in a miRNA duplex, can have significant effects on the efficiency of the plant antiviral immune response.
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spelling pubmed-91038042022-05-14 RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants Pertermann, Robert Golbik, Ralph Peter Tamilarasan, Selvaraj Gursinsky, Torsten Gago-Zachert, Selma Pantaleo, Vitantonio Thondorf, Iris Behrens, Sven-Erik Int J Mol Sci Article Many plant viruses express suppressor proteins (VSRs) that can inhibit RNA silencing, a central component of antiviral plant immunity. The most common activity of VSRs is the high-affinity binding of virus-derived siRNAs and thus their sequestration from the silencing process. Since siRNAs share large homologies with miRNAs, VSRs like the Tombusvirus p19 may also bind miRNAs and in this way modulate cellular gene expression at the post-transcriptional level. Interestingly, the binding affinity of p19 varies considerably between different miRNAs, and the molecular determinants affecting this property have not yet been adequately characterized. Addressing this, we analyzed the binding of p19 to the miRNAs 162 and 168, which regulate the expression of the important RNA silencing constituents Dicer-like 1 (DCL1) and Argonaute 1 (AGO1), respectively. p19 binds miRNA162 with similar high affinity as siRNA, whereas the affinity for miRNA168 is significantly lower. We show that specific molecular features, such as mismatches and ‘G–U wobbles’ on the RNA side and defined amino acid residues on the VSR side, mediate this property. Our observations highlight the remarkable adaptation of VSR binding affinities to achieve differential effects on host miRNA activities. Moreover, they show that even minimal changes, i.e., a single base pair in a miRNA duplex, can have significant effects on the efficiency of the plant antiviral immune response. MDPI 2022-04-29 /pmc/articles/PMC9103804/ /pubmed/35563369 http://dx.doi.org/10.3390/ijms23094977 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Pertermann, Robert
Golbik, Ralph Peter
Tamilarasan, Selvaraj
Gursinsky, Torsten
Gago-Zachert, Selma
Pantaleo, Vitantonio
Thondorf, Iris
Behrens, Sven-Erik
RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants
title RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants
title_full RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants
title_fullStr RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants
title_full_unstemmed RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants
title_short RNA and Protein Determinants Mediate Differential Binding of miRNAs by a Viral Suppressor of RNA Silencing Thus Modulating Antiviral Immune Responses in Plants
title_sort rna and protein determinants mediate differential binding of mirnas by a viral suppressor of rna silencing thus modulating antiviral immune responses in plants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9103804/
https://www.ncbi.nlm.nih.gov/pubmed/35563369
http://dx.doi.org/10.3390/ijms23094977
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