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The diversity of Shine-Dalgarno sequences sheds light on the evolution of translation initiation

Journal

RNA BIOLOGY
Volume 18, Issue 11, Pages 1489-1500

Publisher

TAYLOR & FRANCIS INC
DOI: 10.1080/15476286.2020.1861406

Keywords

Shine-Dalgarno sequence; ribosome; mRNA; transcriptome; translation initiation; evolution; diversity

Funding

  1. Ministry of Science and Technology, Taiwan [105-2311-B-002-004-MY2, 106-2628-B-002-002-MY4, 109-2311-B-002-009-MY3]
  2. National Taiwan University (TW) [109L7706, 109L7867, 109L104051]

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The diversity of SD sequences is widespread in prokaryotes, while aSD sequences remain relatively stable. Research has shown that SD:aSD base pairing is beneficial but nonessential to translation initiation, and that the untranslated region of mRNA and ribosomes have evolved distinct ways of translation initiation in different species.
Shine-Dalgarno (SD) sequences, the core element of prokaryotic ribosome-binding sites, facilitate mRNA translation by base-pair interaction with the anti-SD (aSD) sequence of 16S rRNA. In contrast to this paradigm, an inspection of thousands of prokaryotic species unravels tremendous SD sequence diversity both within and between genomes, whereas aSD sequences remain largely static. The pattern has led many to suggest unidentified mechanisms for translation initiation. Here we review known translation-initiation pathways in prokaryotes. Moreover, we seek to understand the cause and consequence of SD diversity through surveying recent advances in biochemistry, genomics, and high-throughput genetics. These findings collectively show: (1) SD:aSD base pairing is beneficial but nonessential to translation initiation. (2) The 5MODIFIER LETTER PRIME untranslated region of mRNA evolves dynamically and correlates with organismal phylogeny and ecological niches. (3) Ribosomes have evolved distinct usage of translation-initiation pathways in different species. We propose a model portraying the SD diversity shaped by optimization of gene expression, adaptation to environments and growth demands, and the species-specific prerequisite of ribosomes to initiate translation. The model highlights the coevolution of ribosomes and mRNA features, leading to functional customization of the translation apparatus in each organism.

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