Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs

ABSTRACT Many viruses produce protein-coding and noncoding subgenomic RNAs (sgRNAs) that are critical for infection. A recently discovered pathway for viral sgRNA production uses exoribonuclease-resistant RNAs (xrRNAs), discrete folded RNA elements that block the processive exoribonucleolytic degrad...

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Autores principales:	Anna-Lena Steckelberg, Quentin Vicens, Jeffrey S. Kieft
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Infernal RNA structure exoribonuclease resistance plant viruses viral RNA Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ed96e129305943a59a98aa98b36203f1
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spelling	oai:doaj.org-article:ed96e129305943a59a98aa98b36203f12021-11-15T15:52:19ZExoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs10.1128/mBio.02461-182150-7511https://doaj.org/article/ed96e129305943a59a98aa98b36203f12018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02461-18https://doaj.org/toc/2150-7511ABSTRACT Many viruses produce protein-coding and noncoding subgenomic RNAs (sgRNAs) that are critical for infection. A recently discovered pathway for viral sgRNA production uses exoribonuclease-resistant RNAs (xrRNAs), discrete folded RNA elements that block the processive exoribonucleolytic degradation of RNA. xrRNAs are widespread in animal-infecting flaviviruses but had been found only in three members of the plant virus genus Dianthovirus. Also, xrRNAs had been found only in the 3′ untranslated regions (3′UTRs) of viral RNAs, where they produce noncoding sgRNAs. The degree to which xrRNA elements exist in other viruses, the conservation of their ring-like fold, and the ability of xrRNAs to operate in diverse contexts were unknown. Using computational tools and biochemical assays, we discovered xrRNA elements pervading two large families of plant-infecting RNA viruses, demonstrating their importance and widespread utility. Comparison of the sequences and functional requirements suggests that all adopt the characteristic ring-like fold. Unexpectedly, many of these newly discovered xrRNAs are located in intergenic regions rather than 3´UTRs, and some are associated with the 5′ ends of subgenomic RNAs that encode viral proteins. This suggests that xrRNAs are involved in the production of both coding and noncoding subgenomic RNAs and can operate as part of broader mechanisms to regulate RNA levels and protein expression. These discoveries expand the potential roles for xrRNAs and suggest that xrRNAs may represent a more general strategy for RNA maturation and maintenance than previously known. IMPORTANCE During infection, viruses often produce subgenomic RNAs (sgRNAs) that either serve as the template for protein synthesis or act as “riboregulators” that interact with and influence the viral and cellular machinery. Recently, a mechanism for producing sgRNAs was found that depends on the presence of specifically structured RNA elements (xrRNAs). However, the degree to which this mechanism is used, where the elements are found, their structural diversity, and what types of sgRNAs are produced by this pathway were unclear. This article describes the discovery of these structured RNA elements in two large families of plant viruses and shows that they are used to produce both protein-coding sgRNAs and “riboregulatory” RNAs. These discoveries provide evidence that xrRNA-based RNA maturation pathways may be more widespread than previously anticipated and that they are involved in producing a variety of RNAs of diverse functions.Anna-Lena SteckelbergQuentin VicensJeffrey S. KieftAmerican Society for MicrobiologyarticleInfernalRNA structureexoribonuclease resistanceplant virusesviral RNAMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Infernal RNA structure exoribonuclease resistance plant viruses viral RNA Microbiology QR1-502
spellingShingle	Infernal RNA structure exoribonuclease resistance plant viruses viral RNA Microbiology QR1-502 Anna-Lena Steckelberg Quentin Vicens Jeffrey S. Kieft Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs
description	ABSTRACT Many viruses produce protein-coding and noncoding subgenomic RNAs (sgRNAs) that are critical for infection. A recently discovered pathway for viral sgRNA production uses exoribonuclease-resistant RNAs (xrRNAs), discrete folded RNA elements that block the processive exoribonucleolytic degradation of RNA. xrRNAs are widespread in animal-infecting flaviviruses but had been found only in three members of the plant virus genus Dianthovirus. Also, xrRNAs had been found only in the 3′ untranslated regions (3′UTRs) of viral RNAs, where they produce noncoding sgRNAs. The degree to which xrRNA elements exist in other viruses, the conservation of their ring-like fold, and the ability of xrRNAs to operate in diverse contexts were unknown. Using computational tools and biochemical assays, we discovered xrRNA elements pervading two large families of plant-infecting RNA viruses, demonstrating their importance and widespread utility. Comparison of the sequences and functional requirements suggests that all adopt the characteristic ring-like fold. Unexpectedly, many of these newly discovered xrRNAs are located in intergenic regions rather than 3´UTRs, and some are associated with the 5′ ends of subgenomic RNAs that encode viral proteins. This suggests that xrRNAs are involved in the production of both coding and noncoding subgenomic RNAs and can operate as part of broader mechanisms to regulate RNA levels and protein expression. These discoveries expand the potential roles for xrRNAs and suggest that xrRNAs may represent a more general strategy for RNA maturation and maintenance than previously known. IMPORTANCE During infection, viruses often produce subgenomic RNAs (sgRNAs) that either serve as the template for protein synthesis or act as “riboregulators” that interact with and influence the viral and cellular machinery. Recently, a mechanism for producing sgRNAs was found that depends on the presence of specifically structured RNA elements (xrRNAs). However, the degree to which this mechanism is used, where the elements are found, their structural diversity, and what types of sgRNAs are produced by this pathway were unclear. This article describes the discovery of these structured RNA elements in two large families of plant viruses and shows that they are used to produce both protein-coding sgRNAs and “riboregulatory” RNAs. These discoveries provide evidence that xrRNA-based RNA maturation pathways may be more widespread than previously anticipated and that they are involved in producing a variety of RNAs of diverse functions.
format	article
author	Anna-Lena Steckelberg Quentin Vicens Jeffrey S. Kieft
author_facet	Anna-Lena Steckelberg Quentin Vicens Jeffrey S. Kieft
author_sort	Anna-Lena Steckelberg
title	Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs
title_short	Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs
title_full	Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs
title_fullStr	Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs
title_full_unstemmed	Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs
title_sort	exoribonuclease-resistant rnas exist within both coding and noncoding subgenomic rnas
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/ed96e129305943a59a98aa98b36203f1
work_keys_str_mv	AT annalenasteckelberg exoribonucleaseresistantrnasexistwithinbothcodingandnoncodingsubgenomicrnas AT quentinvicens exoribonucleaseresistantrnasexistwithinbothcodingandnoncodingsubgenomicrnas AT jeffreyskieft exoribonucleaseresistantrnasexistwithinbothcodingandnoncodingsubgenomicrnas
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Exoribonuclease-Resistant RNAs Exist within both Coding and Noncoding Subgenomic RNAs

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