Suppression of RNAi by dsRNA-Degrading RNaseIII Enzymes of Viruses in Animals and Plants

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Weinheimer , I , Jiu , Y , Rajamäki , M , Matilainen , O , Kallijärvi , J , Cuellar , W , Lu , R , Saarma , M , Holmberg , C I , Jäntti , J & Valkonen , J 2015 , ' Suppression of RNAi by dsRNA-Degrading RNaseIII Enzymes of Viruses in Animals and Plants ' , PLoS Pathogens , vol. 11 , no. 3 , e1004711 .

Title: Suppression of RNAi by dsRNA-Degrading RNaseIII Enzymes of Viruses in Animals and Plants
Author: Weinheimer, Isabel; Jiu, Yaming; Rajamäki, Minna; Matilainen, Olli; Kallijärvi, Jukka; Cuellar, Wilmer; Lu, Rui; Saarma, Mart; Holmberg, Carina I; Jäntti, Jussi; Valkonen, Jari
Contributor organization: Department of Agricultural Sciences
Institute of Biotechnology
Research Programs Unit
Translational Cancer Biology (TCB) Research Programme
Department of Biochemistry and Developmental Biology
Viikki Plant Science Centre (ViPS)
Plant Pathology and Virology
Plant Production Sciences
Date: 2015-03-06
Language: eng
Number of pages: 25
Belongs to series: PLoS Pathogens
ISSN: 1553-7366
Abstract: Certain RNA and DNA viruses that infect plants, insects, fish or poikilothermic animals encode Class 1 RNaseIII endoribonuclease-like proteins. dsRNA-specific endoribonuclease activity of the RNaseIII of rock bream iridovirus infecting fish and Sweet potato chlorotic stunt crinivirus (SPCSV) infecting plants has been shown. Suppression of the host antiviral RNA interference (RNAi) pathway has been documented with the RNaseIII of SPCSV and Heliothis virescens ascovirus infecting insects. Suppression of RNAi by the viral RNaseIIIs in non-host organisms of different kingdoms is not known. Here we expressed PPR3, the RNaseIII of Pike-perch iridovirus, in the non-hosts Nicotiana benthamiana (plant) and Caenorhabditis elegans (nematode) and found that it cleaves double-stranded small interfering RNA (ds-siRNA) molecules that are pivotal in the host RNA interference (RNAi) pathway and thereby suppresses RNAi in non-host tissues. In N. benthamiana, PPR3 enhanced accumulation of Tobacco rattle tobravirus RNA1 replicon lacking the 16K RNAi suppressor. Furthermore, PPR3 suppressed single-stranded RNA (ssRNA)–mediated RNAi and rescued replication of Flock House virus RNA1 replicon lacking the B2 RNAi suppressor in C. elegans. Suppression of RNAi was debilitated with the catalytically compromised mutant PPR3-Ala. However, the RNaseIII (CSR3) produced by SPCSV, which cleaves ds-siRNA and counteracts antiviral RNAi in plants, failed to suppress ssRNA-mediated RNAi in C. elegans. In leaves of N. benthamiana, PPR3 suppressed RNAi induced by ssRNA and dsRNA and reversed silencing; CSR3, however, suppressed only RNAi induced by ssRNA and was unable to reverse silencing. Neither PPR3 nor CSR3 suppressed antisense-mediated RNAi in Drosophila melanogaster. These results show that the RNaseIII enzymes of RNA and DNA viruses suppress RNAi, which requires catalytic activities of RNaseIII. In contrast to other viral silencing suppression proteins, the RNaseIII enzymes are homologous in unrelated RNA and DNA viruses and can be detected in viral genomes using gene modeling and protein structure prediction programs.
Subject: 1183 Plant biology, microbiology, virology
3111 Biomedicine
Peer reviewed: Yes
Usage restriction: openAccess
Self-archived version: publishedVersion

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