Identification of herpesvirus transcripts from genomic regions around the replication origins

Abstract Long-read sequencing (LRS) techniques enable the identification of full-length RNA molecules in a single run eliminating the need for additional assembly steps. LRS research has exposed unanticipated transcriptomic complexity in various organisms, including viruses. Herpesviruses are known...

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Main Authors: Gábor Torma, Dóra Tombácz, Zsolt Csabai, Islam A. A. Almsarrhad, Gergely Ármin Nagy, Balázs Kakuk, Gábor Gulyás, Lauren McKenzie Spires, Ishaan Gupta, Ádám Fülöp, Ákos Dörmő, István Prazsák, Máté Mizik, Virág Éva Dani, Viktor Csányi, Ákos Harangozó, Zoltán Zádori, Zsolt Toth, Zsolt Boldogkői
Format: Article
Language:English
Published: Nature Portfolio 2023-09-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-43344-y
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author Gábor Torma
Dóra Tombácz
Zsolt Csabai
Islam A. A. Almsarrhad
Gergely Ármin Nagy
Balázs Kakuk
Gábor Gulyás
Lauren McKenzie Spires
Ishaan Gupta
Ádám Fülöp
Ákos Dörmő
István Prazsák
Máté Mizik
Virág Éva Dani
Viktor Csányi
Ákos Harangozó
Zoltán Zádori
Zsolt Toth
Zsolt Boldogkői
author_facet Gábor Torma
Dóra Tombácz
Zsolt Csabai
Islam A. A. Almsarrhad
Gergely Ármin Nagy
Balázs Kakuk
Gábor Gulyás
Lauren McKenzie Spires
Ishaan Gupta
Ádám Fülöp
Ákos Dörmő
István Prazsák
Máté Mizik
Virág Éva Dani
Viktor Csányi
Ákos Harangozó
Zoltán Zádori
Zsolt Toth
Zsolt Boldogkői
author_sort Gábor Torma
collection DOAJ
description Abstract Long-read sequencing (LRS) techniques enable the identification of full-length RNA molecules in a single run eliminating the need for additional assembly steps. LRS research has exposed unanticipated transcriptomic complexity in various organisms, including viruses. Herpesviruses are known to produce a range of transcripts, either close to or overlapping replication origins (Oris) and neighboring genes related to transcription or replication, which possess confirmed or potential regulatory roles. In our research, we employed both new and previously published LRS and short-read sequencing datasets to uncover additional Ori-proximal transcripts in nine herpesviruses from all three subfamilies (alpha, beta and gamma). We discovered novel long non-coding RNAs, as well as splice and length isoforms of mRNAs. Moreover, our analysis uncovered an intricate network of transcriptional overlaps within the examined genomic regions. We demonstrated that herpesviruses display distinct patterns of transcriptional overlaps in the vicinity of or at the Oris. Our findings suggest the existence of a ‘super regulatory center’ in the genome of alphaherpesviruses that governs the initiation of both DNA replication and global transcription through multilayered interactions among the molecular machineries.
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spelling doaj.art-06e84a45cae64350bc7931c004d3aef52023-11-19T12:59:42ZengNature PortfolioScientific Reports2045-23222023-09-0113112510.1038/s41598-023-43344-yIdentification of herpesvirus transcripts from genomic regions around the replication originsGábor Torma0Dóra Tombácz1Zsolt Csabai2Islam A. A. Almsarrhad3Gergely Ármin Nagy4Balázs Kakuk5Gábor Gulyás6Lauren McKenzie Spires7Ishaan Gupta8Ádám Fülöp9Ákos Dörmő10István Prazsák11Máté Mizik12Virág Éva Dani13Viktor Csányi14Ákos Harangozó15Zoltán Zádori16Zsolt Toth17Zsolt Boldogkői18Department of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Oral Biology, University of Florida College of DentistryDepartment of Biochemical Engineering and Biotechnology, Indian Institute of TechnologyDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedHUN-REN Veterinary Medical Research Institute HUDepartment of Oral Biology, University of Florida College of DentistryDepartment of Medical Biology, Albert Szent-Györgyi Medical School, University of SzegedAbstract Long-read sequencing (LRS) techniques enable the identification of full-length RNA molecules in a single run eliminating the need for additional assembly steps. LRS research has exposed unanticipated transcriptomic complexity in various organisms, including viruses. Herpesviruses are known to produce a range of transcripts, either close to or overlapping replication origins (Oris) and neighboring genes related to transcription or replication, which possess confirmed or potential regulatory roles. In our research, we employed both new and previously published LRS and short-read sequencing datasets to uncover additional Ori-proximal transcripts in nine herpesviruses from all three subfamilies (alpha, beta and gamma). We discovered novel long non-coding RNAs, as well as splice and length isoforms of mRNAs. Moreover, our analysis uncovered an intricate network of transcriptional overlaps within the examined genomic regions. We demonstrated that herpesviruses display distinct patterns of transcriptional overlaps in the vicinity of or at the Oris. Our findings suggest the existence of a ‘super regulatory center’ in the genome of alphaherpesviruses that governs the initiation of both DNA replication and global transcription through multilayered interactions among the molecular machineries.https://doi.org/10.1038/s41598-023-43344-y
spellingShingle Gábor Torma
Dóra Tombácz
Zsolt Csabai
Islam A. A. Almsarrhad
Gergely Ármin Nagy
Balázs Kakuk
Gábor Gulyás
Lauren McKenzie Spires
Ishaan Gupta
Ádám Fülöp
Ákos Dörmő
István Prazsák
Máté Mizik
Virág Éva Dani
Viktor Csányi
Ákos Harangozó
Zoltán Zádori
Zsolt Toth
Zsolt Boldogkői
Identification of herpesvirus transcripts from genomic regions around the replication origins
Scientific Reports
title Identification of herpesvirus transcripts from genomic regions around the replication origins
title_full Identification of herpesvirus transcripts from genomic regions around the replication origins
title_fullStr Identification of herpesvirus transcripts from genomic regions around the replication origins
title_full_unstemmed Identification of herpesvirus transcripts from genomic regions around the replication origins
title_short Identification of herpesvirus transcripts from genomic regions around the replication origins
title_sort identification of herpesvirus transcripts from genomic regions around the replication origins
url https://doi.org/10.1038/s41598-023-43344-y
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