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Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement

Overlapping genes (OGs) are a universal phenomenon in all kingdoms, and viruses display a high content of OGs combined with a high rate of evolution. It is believed that the mechanism of gene overlap is based on overprinting of an existing gene. OGs help virus genes compress a maximum amount of info...

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Autores principales: Dorokhov, Yuri L., Sheshukova, Ekaterina V., Komarova, Tatiana V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5425575/
https://www.ncbi.nlm.nih.gov/pubmed/28553276
http://dx.doi.org/10.3389/fmicb.2017.00851
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author Dorokhov, Yuri L.
Sheshukova, Ekaterina V.
Komarova, Tatiana V.
author_facet Dorokhov, Yuri L.
Sheshukova, Ekaterina V.
Komarova, Tatiana V.
author_sort Dorokhov, Yuri L.
collection PubMed
description Overlapping genes (OGs) are a universal phenomenon in all kingdoms, and viruses display a high content of OGs combined with a high rate of evolution. It is believed that the mechanism of gene overlap is based on overprinting of an existing gene. OGs help virus genes compress a maximum amount of information into short sequences, conferring viral proteins with novel features and thereby increasing their within-host fitness. Analysis of tobamovirus 3′-terminal genes reveals at least two modes of OG organization and mechanisms of interaction with the host. Originally isolated from Solanaceae species, viruses (referred to as Solanaceae-infecting) such as tobacco mosaic virus do not show 3′-terminal overlap between movement protein (MP) and coat protein (CP) genes but do contain open reading frame 6 (ORF6), which overlaps with both genes. Conversely, tobamoviruses, originally isolated from Brassicaceae species (referred to as Brassicaceae-infecting) and also able to infect Solanaceae plants, have no ORF6 but are characterized by overlapping MP and CP genes. Our analysis showed that the MP/CP overlap of Brassicaceae-infecting tobamoviruses results in the following: (i) genome compression and strengthening of subgenomic promoters; (ii) CP gene early expression directly from genomic and dicistronic MP subgenomic mRNA using an internal ribosome entry site (IRES) and a stable hairpin structure in the overlapping region; (iii) loss of ORF6, which influences the symptomatology of Solanaceae-infecting tobamoviruses; and (iv) acquisition of an IRES polypurine-rich region encoding an MP nuclear localization signal. We believe that MP/CP gene overlap may constitute a mechanism for host range expansion and virus adjustment to Brassicaceae plants.
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spelling pubmed-54255752017-05-26 Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement Dorokhov, Yuri L. Sheshukova, Ekaterina V. Komarova, Tatiana V. Front Microbiol Microbiology Overlapping genes (OGs) are a universal phenomenon in all kingdoms, and viruses display a high content of OGs combined with a high rate of evolution. It is believed that the mechanism of gene overlap is based on overprinting of an existing gene. OGs help virus genes compress a maximum amount of information into short sequences, conferring viral proteins with novel features and thereby increasing their within-host fitness. Analysis of tobamovirus 3′-terminal genes reveals at least two modes of OG organization and mechanisms of interaction with the host. Originally isolated from Solanaceae species, viruses (referred to as Solanaceae-infecting) such as tobacco mosaic virus do not show 3′-terminal overlap between movement protein (MP) and coat protein (CP) genes but do contain open reading frame 6 (ORF6), which overlaps with both genes. Conversely, tobamoviruses, originally isolated from Brassicaceae species (referred to as Brassicaceae-infecting) and also able to infect Solanaceae plants, have no ORF6 but are characterized by overlapping MP and CP genes. Our analysis showed that the MP/CP overlap of Brassicaceae-infecting tobamoviruses results in the following: (i) genome compression and strengthening of subgenomic promoters; (ii) CP gene early expression directly from genomic and dicistronic MP subgenomic mRNA using an internal ribosome entry site (IRES) and a stable hairpin structure in the overlapping region; (iii) loss of ORF6, which influences the symptomatology of Solanaceae-infecting tobamoviruses; and (iv) acquisition of an IRES polypurine-rich region encoding an MP nuclear localization signal. We believe that MP/CP gene overlap may constitute a mechanism for host range expansion and virus adjustment to Brassicaceae plants. Frontiers Media S.A. 2017-05-11 /pmc/articles/PMC5425575/ /pubmed/28553276 http://dx.doi.org/10.3389/fmicb.2017.00851 Text en Copyright © 2017 Dorokhov, Sheshukova and Komarova. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Dorokhov, Yuri L.
Sheshukova, Ekaterina V.
Komarova, Tatiana V.
Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement
title Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement
title_full Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement
title_fullStr Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement
title_full_unstemmed Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement
title_short Tobamovirus 3′-Terminal Gene Overlap May be a Mechanism for within-Host Fitness Improvement
title_sort tobamovirus 3′-terminal gene overlap may be a mechanism for within-host fitness improvement
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5425575/
https://www.ncbi.nlm.nih.gov/pubmed/28553276
http://dx.doi.org/10.3389/fmicb.2017.00851
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