1,103
Views
2
CrossRef citations to date
0
Altmetric
Research Paper

Prokaryotic rRNA-mRNA interactions are involved in all translation steps and shape bacterial transcripts

, , , , , & show all
Pages 684-698 | Received 10 Apr 2021, Accepted 06 Sep 2021, Published online: 29 Sep 2021

References

  • Shine J, Dalgarno L. Determinant of cistron specificity in bacterial ribosomes. Nature. 1975;254(5495):34–38.
  • Kozak M. Initiation of translation in prokaryotes and eukaryotes. Gene. 1999;234(2):187–208.
  • Nakagawa S, Niimura Y, Miura KL, et al. Dynamic evolution of translation initiation mechanisms in prokaryotes. Proc Natl Acad Sci. 2010;107(14):6382–6387.
  • Shine J, Dalgarno L. The 3’-Terminal sequence of escherichia coli 16S Ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci. 1974;71(4):1342–1346.
  • Li GW, Oh E, Weissman JS. The anti-Shine–Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature. 2012;484(7395):538–541.
  • Liu X, Jiang H, Gu Z, et al. High-resolution view of bacteriophage lambda gene expression by ribosome profiling. Proc Natl Acad Sci. 2013 Jul;110(29):11928–11933.
  • Schrader JM, Zhou B, Li G-W, et al. The coding and noncoding architecture of the caulobacter crescentus genome. PLoS Genetics. 2014 Jul;10(7):e1004463.
  • Diwan GD, Agashe D. The frequency of Internal Shine–Dalgarno-like motifs in prokaryotes. Genome Biol Evol. 2016;8(6):1722–1733.
  • Hockenberry AJ, Jewett MC, Amaral LAN, et al. Within-Gene Shine–Dalgarno sequences are not selected for function. Mol Biol Evol. 2018;35(10):2487–2498.
  • Buttgereit F, Brand MD. A hierarchy of ATP-consuming processes in mammalian cells. Biochem J. 1995;312(1):163–167.
  • Lane N, Martin W. The energetics of genome complexity. Nature. 2010;467(7318):929–934.
  • Tuller T, Carmi A, Vestsigian K, et al. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell. 2010;141(2):344–354.
  • Tuller T, Zur H. Multiple roles of the coding sequence 5′ end in gene expression regulation. Nucleic Acids Research. 2015;43(1):13–28.
  • Fredrick K, Ibba M. How the sequence of a gene can tune its translation. Cell. 2010;141(2):227–229.
  • Yang C, Hockenberry AJ, Jewett MC. Depletion of shine-dalgarno sequences within bacterial coding regions is expression dependent. G3 Genes|Genomes|Genetics. 2016;6(November):3467–3474.
  • Salis HM, Mirsky EA, Voigt CA. Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol. 2009;27(10):946–950.
  • Márquez V, Wilson DN, Tate WP, et al. Maintaining the ribosomal reading frame: the influence of the E site during translational regulation of release factor 2. Cell. 2004;118(1):45–55.
  • Korostelev A, Trakhanov S, Asahara H, et al. Interactions and dynamics of the Shine Dalgarno helix in the 70S ribosome. Proc Natl Acad Sci U S A. 2007;104(43):16840–16843.
  • Weiner I, Shahar N, Marco P, et al. Solving the riddle of the evolution of shine-dalgarno based translation in chloroplasts. Mol Biol Evol. 2019;36(12):2854–2860.
  • Scharff LB, Childs L, Walther D, et al. Local absence of secondary structure permits translation of mrnas that lack ribosome-binding sites. PLoS Genetics. 2011;7(6):e1002155.
  • Woese CR, Debrunner-Vossbrinck BA, Oyaizu H, et al. Gram-positive bacteria: possible photosynthetic ancestry. Science. 1985;229(4715):762–765.
  • Bergman S, Tuller T. Widespread non-modular overlapping codes in the coding regions. Phys Biol. 2020;17(3):031002.
  • Zur H, Tuller T. Exploiting hidden information interleaved in the redundancy of the genetic code without prior knowledge. Bioinformatics. 2015;31(8):1161–1168.
  • Bahiri-Elitzur S, Tuller T. Computational discovery and modeling of novel gene expression rules encoded in the mRNA. Biochem Soc Trans. 2020;48(4):1519–1528.
  • Zur H, Tuller T. New universal rules of eukaryotic translation initiation fidelity. PLoS Comput Biol. 2013;9(7):e1003136.
  • Bonetti B, Fu L, Moon J, et al. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J Mol Biol. 1995 Aug;251(3):334–345.
  • Dos Reis M, Wernisch L. Estimating translational selection in eukaryotic genomes. Mol Biol Evol. 2009;26(2):451–461.
  • Mohammad F, Woolstenhulme CJ, Green R, et al. Clarifying the translational pausing landscape in bacteria by ribosome profiling. Cell Rep. 2016;14(4):686–694.
  • Peeri M, Tuller T. High-resolution modeling of the selection on local mRNA folding strength in coding sequences across the tree of life. Genome Biol. 2020;21(1). DOI:10.1186/s13059-020-01971-y
  • Kudla G, Murray AW, Tollervey D, et al. Coding-sequence determinants of gene expression in Escherichia coli. Science. 2009;324(5924):255-258.
  • Sharpl PM, Li W. The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987;15(3):1281–1295.
  • Tuller T, Waldman YY, Kupiec M, et al. Translation efficiency is determined by both codon bias and folding energy. Proc Natl Acad Sci. 2010;107(8):3645–3650.
  • Bernstein JA, Khodursky AB, Lin P-H, et al. Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci. 2002 Jul;99(15):9697–9702.
  • Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, et al. Translation-independent localization of mRNA in E. coli. Science. 2011;331(6020):1081–1084.
  • Yurovsky A, Amin MR, Gardin J, et al. Prokaryotic coding regions have little if any specific depletion of Shine-Dalgarno motifsPLoS One. 2018 Aug 23;13(8):e0202768.
  • Hockenberry AJ, Amaral AN, Jewett MC, et al. Selection removes Shine-Dalgarno-like sequences from within protein coding genes Assessing the conservation status of Shine-Dalgarno-like sequenceMol Biol Evol. 2018;35(10):2487-2498.
  • Shaham G, Tuller T. Genome scale analysis of Escherichia coli with a comprehensive prokaryotic sequence-based biophysical model of translation initiation and elongation. DNA Res. 2018;25(2):195–205.
  • Hofacker IL. Vienna RNA secondary structure server.
  • Diament A, Tuller T. Estimation of ribosome profiling performance and reproducibility at various levels of resolution. Biol Direct. 2016;11(1):24.
  • MartinRemoves adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011 May;17(1):10–12.
  • Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009 Mar;10(3):R25.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.