The footprint of genome architecture in the largest genome expansion in RNA viruses.

The small size of RNA virus genomes (2-to-32 kb) has been attributed to high mutation rates during replication, which is thought to lack proof-reading. This paradigm is being revisited owing to the discovery of a 3'-to-5' exoribonuclease (ExoN) in nidoviruses, a monophyletic group of posit...

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Autores principales:	Chris Lauber, Jelle J Goeman, Maria del Carmen Parquet, Phan Thi Nga, Eric J Snijder, Kouichi Morita, Alexander E Gorbalenya
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/ffe37aa6492648b288f00d6c33ddf777
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spelling	oai:doaj.org-article:ffe37aa6492648b288f00d6c33ddf7772021-11-18T06:05:22ZThe footprint of genome architecture in the largest genome expansion in RNA viruses.1553-73661553-737410.1371/journal.ppat.1003500https://doaj.org/article/ffe37aa6492648b288f00d6c33ddf7772013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23874204/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The small size of RNA virus genomes (2-to-32 kb) has been attributed to high mutation rates during replication, which is thought to lack proof-reading. This paradigm is being revisited owing to the discovery of a 3'-to-5' exoribonuclease (ExoN) in nidoviruses, a monophyletic group of positive-stranded RNA viruses with a conserved genome architecture. ExoN, a homolog of canonical DNA proof-reading enzymes, is exclusively encoded by nidoviruses with genomes larger than 20 kb. All other known non-segmented RNA viruses have smaller genomes. Here we use evolutionary analyses to show that the two- to three-fold expansion of the nidovirus genome was accompanied by a large number of replacements in conserved proteins at a scale comparable to that in the Tree of Life. To unravel common evolutionary patterns in such genetically diverse viruses, we established the relation between genomic regions in nidoviruses in a sequence alignment-free manner. We exploited the conservation of the genome architecture to partition each genome into five non-overlapping regions: 5' untranslated region (UTR), open reading frame (ORF) 1a, ORF1b, 3'ORFs (encompassing the 3'-proximal ORFs), and 3' UTR. Each region was analyzed for its contribution to genome size change under different models. The non-linear model statistically outperformed the linear one and captured >92% of data variation. Accordingly, nidovirus genomes were concluded to have reached different points on an expansion trajectory dominated by consecutive increases of ORF1b, ORF1a, and 3'ORFs. Our findings indicate a unidirectional hierarchical relation between these genome regions, which are distinguished by their expression mechanism. In contrast, these regions cooperate bi-directionally on a functional level in the virus life cycle, in which they predominantly control genome replication, genome expression, and virus dissemination, respectively. Collectively, our findings suggest that genome architecture and the associated region-specific division of labor leave a footprint on genome expansion and may limit RNA genome size.Chris LauberJelle J GoemanMaria del Carmen ParquetPhan Thi NgaEric J SnijderKouichi MoritaAlexander E GorbalenyaPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 9, Iss 7, p e1003500 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Chris Lauber Jelle J Goeman Maria del Carmen Parquet Phan Thi Nga Eric J Snijder Kouichi Morita Alexander E Gorbalenya The footprint of genome architecture in the largest genome expansion in RNA viruses.
description	The small size of RNA virus genomes (2-to-32 kb) has been attributed to high mutation rates during replication, which is thought to lack proof-reading. This paradigm is being revisited owing to the discovery of a 3'-to-5' exoribonuclease (ExoN) in nidoviruses, a monophyletic group of positive-stranded RNA viruses with a conserved genome architecture. ExoN, a homolog of canonical DNA proof-reading enzymes, is exclusively encoded by nidoviruses with genomes larger than 20 kb. All other known non-segmented RNA viruses have smaller genomes. Here we use evolutionary analyses to show that the two- to three-fold expansion of the nidovirus genome was accompanied by a large number of replacements in conserved proteins at a scale comparable to that in the Tree of Life. To unravel common evolutionary patterns in such genetically diverse viruses, we established the relation between genomic regions in nidoviruses in a sequence alignment-free manner. We exploited the conservation of the genome architecture to partition each genome into five non-overlapping regions: 5' untranslated region (UTR), open reading frame (ORF) 1a, ORF1b, 3'ORFs (encompassing the 3'-proximal ORFs), and 3' UTR. Each region was analyzed for its contribution to genome size change under different models. The non-linear model statistically outperformed the linear one and captured >92% of data variation. Accordingly, nidovirus genomes were concluded to have reached different points on an expansion trajectory dominated by consecutive increases of ORF1b, ORF1a, and 3'ORFs. Our findings indicate a unidirectional hierarchical relation between these genome regions, which are distinguished by their expression mechanism. In contrast, these regions cooperate bi-directionally on a functional level in the virus life cycle, in which they predominantly control genome replication, genome expression, and virus dissemination, respectively. Collectively, our findings suggest that genome architecture and the associated region-specific division of labor leave a footprint on genome expansion and may limit RNA genome size.
format	article
author	Chris Lauber Jelle J Goeman Maria del Carmen Parquet Phan Thi Nga Eric J Snijder Kouichi Morita Alexander E Gorbalenya
author_facet	Chris Lauber Jelle J Goeman Maria del Carmen Parquet Phan Thi Nga Eric J Snijder Kouichi Morita Alexander E Gorbalenya
author_sort	Chris Lauber
title	The footprint of genome architecture in the largest genome expansion in RNA viruses.
title_short	The footprint of genome architecture in the largest genome expansion in RNA viruses.
title_full	The footprint of genome architecture in the largest genome expansion in RNA viruses.
title_fullStr	The footprint of genome architecture in the largest genome expansion in RNA viruses.
title_full_unstemmed	The footprint of genome architecture in the largest genome expansion in RNA viruses.
title_sort	footprint of genome architecture in the largest genome expansion in rna viruses.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/ffe37aa6492648b288f00d6c33ddf777
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The footprint of genome architecture in the largest genome expansion in RNA viruses.

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