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The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes

In prokaryotes, translation initiation typically depends on complementary binding between a G-rich Shine–Dalgarno (SD) motif in the 5′ untranslated region of mRNAs, and the 3′ tail of the 16S ribosomal RNA (the anti-SD sequence). In some cases, internal SD-like motifs in the coding region generate “...

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Autores principales: Diwan, Gaurav D, Agashe, Deepa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4943179/
https://www.ncbi.nlm.nih.gov/pubmed/27189998
http://dx.doi.org/10.1093/gbe/evw107
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author Diwan, Gaurav D
Agashe, Deepa
author_facet Diwan, Gaurav D
Agashe, Deepa
author_sort Diwan, Gaurav D
collection PubMed
description In prokaryotes, translation initiation typically depends on complementary binding between a G-rich Shine–Dalgarno (SD) motif in the 5′ untranslated region of mRNAs, and the 3′ tail of the 16S ribosomal RNA (the anti-SD sequence). In some cases, internal SD-like motifs in the coding region generate “programmed” ribosomal pauses that are beneficial for protein folding or accurate targeting. On the other hand, such pauses can also reduce protein production, generating purifying selection against internal SD-like motifs. This selection should be stronger in GC-rich genomes that are more likely to harbor the G-rich SD motif. However, the nature and consequences of selection acting on internal SD-like motifs within genomes and across species remains unclear. We analyzed the frequency of SD-like hexamers in the coding regions of 284 prokaryotes (277 with known anti-SD sequences and 7 without a typical SD mechanism). After accounting for GC content, we found that internal SD-like hexamers are avoided in 230 species, including three without a typical SD mechanism. The degree of avoidance was higher in GC-rich genomes, mesophiles, and N-terminal regions of genes. In contrast, 54 species either showed no signature of avoidance or were enriched in internal SD-like motifs. C-terminal gene regions were relatively enriched in SD-like hexamers, particularly for genes in operons or those followed closely by downstream genes. Together, our results suggest that the frequency of internal SD-like hexamers is governed by multiple factors including GC content and genome organization, and further empirical work is necessary to understand the evolution and functional roles of these motifs.
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spelling pubmed-49431792016-07-14 The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes Diwan, Gaurav D Agashe, Deepa Genome Biol Evol Research Article In prokaryotes, translation initiation typically depends on complementary binding between a G-rich Shine–Dalgarno (SD) motif in the 5′ untranslated region of mRNAs, and the 3′ tail of the 16S ribosomal RNA (the anti-SD sequence). In some cases, internal SD-like motifs in the coding region generate “programmed” ribosomal pauses that are beneficial for protein folding or accurate targeting. On the other hand, such pauses can also reduce protein production, generating purifying selection against internal SD-like motifs. This selection should be stronger in GC-rich genomes that are more likely to harbor the G-rich SD motif. However, the nature and consequences of selection acting on internal SD-like motifs within genomes and across species remains unclear. We analyzed the frequency of SD-like hexamers in the coding regions of 284 prokaryotes (277 with known anti-SD sequences and 7 without a typical SD mechanism). After accounting for GC content, we found that internal SD-like hexamers are avoided in 230 species, including three without a typical SD mechanism. The degree of avoidance was higher in GC-rich genomes, mesophiles, and N-terminal regions of genes. In contrast, 54 species either showed no signature of avoidance or were enriched in internal SD-like motifs. C-terminal gene regions were relatively enriched in SD-like hexamers, particularly for genes in operons or those followed closely by downstream genes. Together, our results suggest that the frequency of internal SD-like hexamers is governed by multiple factors including GC content and genome organization, and further empirical work is necessary to understand the evolution and functional roles of these motifs. Oxford University Press 2016-05-09 /pmc/articles/PMC4943179/ /pubmed/27189998 http://dx.doi.org/10.1093/gbe/evw107 Text en © The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Diwan, Gaurav D
Agashe, Deepa
The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes
title The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes
title_full The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes
title_fullStr The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes
title_full_unstemmed The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes
title_short The Frequency of Internal Shine–Dalgarno-like Motifs in Prokaryotes
title_sort frequency of internal shine–dalgarno-like motifs in prokaryotes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4943179/
https://www.ncbi.nlm.nih.gov/pubmed/27189998
http://dx.doi.org/10.1093/gbe/evw107
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