A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks
Abstract Background Adenosine deaminase enzymes of the ADAR family are conserved in metazoans. They convert adenine into inosine in dsRNAs and thus alter both structural properties and the coding potential of their substrates. Acting on exogenous dsRNAs, ADAR1 exerts a pro- or anti-viral role in ver...
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ftdoajarticles:oai:doaj.org/article:fc3f18d393f6439aa8898c285bf8ac61 2023-05-15T15:58:55+02:00 A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks Umberto Rosani Chang-Ming Bai Lorenzo Maso Maxwell Shapiro Miriam Abbadi Stefania Domeneghetti Chong-Ming Wang Laura Cendron Thomas MacCarthy Paola Venier 2019-07-01T00:00:00Z https://doi.org/10.1186/s12862-019-1472-6 https://doaj.org/article/fc3f18d393f6439aa8898c285bf8ac61 EN eng BMC http://link.springer.com/article/10.1186/s12862-019-1472-6 https://doaj.org/toc/1471-2148 doi:10.1186/s12862-019-1472-6 1471-2148 https://doaj.org/article/fc3f18d393f6439aa8898c285bf8ac61 BMC Evolutionary Biology, Vol 19, Iss 1, Pp 1-18 (2019) ADAR Malacoherpesvirus OsHV-1 AbHV-1 Mollusks Oysters Evolution QH359-425 article 2019 ftdoajarticles https://doi.org/10.1186/s12862-019-1472-6 2022-12-31T12:37:32Z Abstract Background Adenosine deaminase enzymes of the ADAR family are conserved in metazoans. They convert adenine into inosine in dsRNAs and thus alter both structural properties and the coding potential of their substrates. Acting on exogenous dsRNAs, ADAR1 exerts a pro- or anti-viral role in vertebrates and Drosophila. Results We traced 4 ADAR homologs in 14 lophotrochozoan genomes and we classified them into ADAD, ADAR1 or ADAR2, based on phylogenetic and structural analyses of the enzymatic domain. Using RNA-seq and quantitative real time PCR we demonstrated the upregulation of one ADAR1 homolog in the bivalve Crassostrea gigas and in the gastropod Haliotis diversicolor supertexta during Ostreid herpesvirus-1 or Haliotid herpesvirus-1 infection. Accordingly, we demonstrated an extensive ADAR-mediated editing of viral RNAs. Single nucleotide variation (SNV) profiles obtained by pairing RNA- and DNA-seq data from the viral infected individuals resulted to be mostly compatible with ADAR-mediated A-to-I editing (up to 97%). SNVs occurred at low frequency in genomic hotspots, denoted by the overlapping of viral genes encoded on opposite DNA strands. The SNV sites and their upstream neighbor nucleotide indicated the targeting of selected adenosines. The analysis of viral sequences suggested that, under the pressure of the ADAR editing, the two Malacoherpesviridae genomes have evolved to reduce the number of deamination targets. Conclusions We report, for the first time, evidence of an extensive editing of Malacoherpesviridae RNAs attributable to host ADAR1 enzymes. The analysis of base neighbor preferences, structural features and expression profiles of molluscan ADAR1 supports the conservation of the enzyme function among metazoans and further suggested that ADAR1 exerts an antiviral role in mollusks. Article in Journal/Newspaper Crassostrea gigas Directory of Open Access Journals: DOAJ Articles BMC Evolutionary Biology 19 1 |
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Open Polar |
collection |
Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
ADAR Malacoherpesvirus OsHV-1 AbHV-1 Mollusks Oysters Evolution QH359-425 |
spellingShingle |
ADAR Malacoherpesvirus OsHV-1 AbHV-1 Mollusks Oysters Evolution QH359-425 Umberto Rosani Chang-Ming Bai Lorenzo Maso Maxwell Shapiro Miriam Abbadi Stefania Domeneghetti Chong-Ming Wang Laura Cendron Thomas MacCarthy Paola Venier A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks |
topic_facet |
ADAR Malacoherpesvirus OsHV-1 AbHV-1 Mollusks Oysters Evolution QH359-425 |
description |
Abstract Background Adenosine deaminase enzymes of the ADAR family are conserved in metazoans. They convert adenine into inosine in dsRNAs and thus alter both structural properties and the coding potential of their substrates. Acting on exogenous dsRNAs, ADAR1 exerts a pro- or anti-viral role in vertebrates and Drosophila. Results We traced 4 ADAR homologs in 14 lophotrochozoan genomes and we classified them into ADAD, ADAR1 or ADAR2, based on phylogenetic and structural analyses of the enzymatic domain. Using RNA-seq and quantitative real time PCR we demonstrated the upregulation of one ADAR1 homolog in the bivalve Crassostrea gigas and in the gastropod Haliotis diversicolor supertexta during Ostreid herpesvirus-1 or Haliotid herpesvirus-1 infection. Accordingly, we demonstrated an extensive ADAR-mediated editing of viral RNAs. Single nucleotide variation (SNV) profiles obtained by pairing RNA- and DNA-seq data from the viral infected individuals resulted to be mostly compatible with ADAR-mediated A-to-I editing (up to 97%). SNVs occurred at low frequency in genomic hotspots, denoted by the overlapping of viral genes encoded on opposite DNA strands. The SNV sites and their upstream neighbor nucleotide indicated the targeting of selected adenosines. The analysis of viral sequences suggested that, under the pressure of the ADAR editing, the two Malacoherpesviridae genomes have evolved to reduce the number of deamination targets. Conclusions We report, for the first time, evidence of an extensive editing of Malacoherpesviridae RNAs attributable to host ADAR1 enzymes. The analysis of base neighbor preferences, structural features and expression profiles of molluscan ADAR1 supports the conservation of the enzyme function among metazoans and further suggested that ADAR1 exerts an antiviral role in mollusks. |
format |
Article in Journal/Newspaper |
author |
Umberto Rosani Chang-Ming Bai Lorenzo Maso Maxwell Shapiro Miriam Abbadi Stefania Domeneghetti Chong-Ming Wang Laura Cendron Thomas MacCarthy Paola Venier |
author_facet |
Umberto Rosani Chang-Ming Bai Lorenzo Maso Maxwell Shapiro Miriam Abbadi Stefania Domeneghetti Chong-Ming Wang Laura Cendron Thomas MacCarthy Paola Venier |
author_sort |
Umberto Rosani |
title |
A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks |
title_short |
A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks |
title_full |
A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks |
title_fullStr |
A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks |
title_full_unstemmed |
A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks |
title_sort |
a-to-i editing of malacoherpesviridae rnas supports the antiviral role of adar1 in mollusks |
publisher |
BMC |
publishDate |
2019 |
url |
https://doi.org/10.1186/s12862-019-1472-6 https://doaj.org/article/fc3f18d393f6439aa8898c285bf8ac61 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
BMC Evolutionary Biology, Vol 19, Iss 1, Pp 1-18 (2019) |
op_relation |
http://link.springer.com/article/10.1186/s12862-019-1472-6 https://doaj.org/toc/1471-2148 doi:10.1186/s12862-019-1472-6 1471-2148 https://doaj.org/article/fc3f18d393f6439aa8898c285bf8ac61 |
op_doi |
https://doi.org/10.1186/s12862-019-1472-6 |
container_title |
BMC Evolutionary Biology |
container_volume |
19 |
container_issue |
1 |
_version_ |
1766394687503990784 |