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Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus

Piwi-interacting RNAs (piRNAs) are a class of small RNAs primarily responsible for silencing transposons in the animal germ line. The ping-pong cycle, the posttranscriptional silencing branch of the piRNA pathway, relies on piRNAs produced from endogenous transposon remnants to direct cleavage of tr...

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Autores principales: Nigg, Jared C., Kuo, Yen-Wen, Falk, Bryce W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7527727/
https://www.ncbi.nlm.nih.gov/pubmed/32994324
http://dx.doi.org/10.1128/mBio.02209-20
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author Nigg, Jared C.
Kuo, Yen-Wen
Falk, Bryce W.
author_facet Nigg, Jared C.
Kuo, Yen-Wen
Falk, Bryce W.
author_sort Nigg, Jared C.
collection PubMed
description Piwi-interacting RNAs (piRNAs) are a class of small RNAs primarily responsible for silencing transposons in the animal germ line. The ping-pong cycle, the posttranscriptional silencing branch of the piRNA pathway, relies on piRNAs produced from endogenous transposon remnants to direct cleavage of transposon RNA via association with Piwi-family Argonaute proteins. In some mosquito species and mosquito-derived cell lines expressing a functionally expanded group of Piwi-family Argonaute proteins, both RNA and DNA viruses are targeted by piRNAs in a manner thought to involve direct processing of exogenous viral RNA into piRNAs. Whether viruses are targeted by piRNAs in nonmosquito species is unknown. Partial integrations of DNA and nonretroviral RNA virus genomes, termed endogenous viral elements (EVEs), are abundant in arthropod genomes and often produce piRNAs that are speculated to target cognate viruses through the ping-pong cycle. Here, we describe a Diaphorina citri densovirus (DcDV)-derived EVE in the genome of Diaphorina citri. We found that this EVE gives rise to DcDV-specific primary piRNAs and is unevenly distributed among D. citri populations. Unexpectedly, we found that DcDV is targeted by ping-pong-dependent virus-derived piRNAs (vpiRNAs) in D. citri lacking the DcDV-derived EVE, while four naturally infecting RNA viruses of D. citri are not targeted by vpiRNAs. Furthermore, a recombinant Cricket paralysis virus containing a portion of the DcDV genome corresponding to the DcDV-derived EVE was not targeted by vpiRNAs during infection in D. citri harboring the EVE. These results demonstrate that viruses can be targeted by piRNAs in a nonmosquito species independently of endogenous piRNAs.
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spelling pubmed-75277272020-10-19 Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus Nigg, Jared C. Kuo, Yen-Wen Falk, Bryce W. mBio Research Article Piwi-interacting RNAs (piRNAs) are a class of small RNAs primarily responsible for silencing transposons in the animal germ line. The ping-pong cycle, the posttranscriptional silencing branch of the piRNA pathway, relies on piRNAs produced from endogenous transposon remnants to direct cleavage of transposon RNA via association with Piwi-family Argonaute proteins. In some mosquito species and mosquito-derived cell lines expressing a functionally expanded group of Piwi-family Argonaute proteins, both RNA and DNA viruses are targeted by piRNAs in a manner thought to involve direct processing of exogenous viral RNA into piRNAs. Whether viruses are targeted by piRNAs in nonmosquito species is unknown. Partial integrations of DNA and nonretroviral RNA virus genomes, termed endogenous viral elements (EVEs), are abundant in arthropod genomes and often produce piRNAs that are speculated to target cognate viruses through the ping-pong cycle. Here, we describe a Diaphorina citri densovirus (DcDV)-derived EVE in the genome of Diaphorina citri. We found that this EVE gives rise to DcDV-specific primary piRNAs and is unevenly distributed among D. citri populations. Unexpectedly, we found that DcDV is targeted by ping-pong-dependent virus-derived piRNAs (vpiRNAs) in D. citri lacking the DcDV-derived EVE, while four naturally infecting RNA viruses of D. citri are not targeted by vpiRNAs. Furthermore, a recombinant Cricket paralysis virus containing a portion of the DcDV genome corresponding to the DcDV-derived EVE was not targeted by vpiRNAs during infection in D. citri harboring the EVE. These results demonstrate that viruses can be targeted by piRNAs in a nonmosquito species independently of endogenous piRNAs. American Society for Microbiology 2020-09-29 /pmc/articles/PMC7527727/ /pubmed/32994324 http://dx.doi.org/10.1128/mBio.02209-20 Text en Copyright © 2020 Nigg et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Nigg, Jared C.
Kuo, Yen-Wen
Falk, Bryce W.
Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus
title Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus
title_full Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus
title_fullStr Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus
title_full_unstemmed Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus
title_short Endogenous Viral Element-Derived Piwi-Interacting RNAs (piRNAs) Are Not Required for Production of Ping-Pong-Dependent piRNAs from Diaphorina citri Densovirus
title_sort endogenous viral element-derived piwi-interacting rnas (pirnas) are not required for production of ping-pong-dependent pirnas from diaphorina citri densovirus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7527727/
https://www.ncbi.nlm.nih.gov/pubmed/32994324
http://dx.doi.org/10.1128/mBio.02209-20
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