Global Importance of RNA Secondary Structures in Protein-coding Sequences

Overview

Journal Bioinformatics

Publisher Oxford University Press

Specialty Biology

Date 2018 Aug 14

PMID 30101307

Citations 13

Authors

Markus Fricke

Ruman Gerst

Bashar Ibrahim

Michael Niepmann

Manja Marz

Affiliations

Soon will be listed here.

Abstract

Motivation: The protein-coding sequences of messenger RNAs are the linear template for translation of the gene sequence into protein. Nevertheless, the RNA can also form secondary structures by intramolecular base-pairing.

Results: We show that the nucleotide distribution within codons is biased in all taxa of life on a global scale. Thereby, RNA secondary structures that require base-pairing between the position 1 of a codon with the position 1 of an opposing codon (here named RNA secondary structure class c1) are under-represented. We conclude that this bias may result from the co-evolution of codon sequence and mRNA secondary structure, suggesting that RNA secondary structures are generally important in protein-coding regions of mRNAs. The above result also implies that codon position 2 has a smaller influence on the amino acid choice than codon position 1.

Supplementary Information: Supplementary data are available at Bioinformatics online.

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References

Pohlmeyer R . The genetic code revisited. J Theor Biol. 2008; 253(3):623-4. DOI: 10.1016/j.jtbi.2008.04.028. View

Berleant D, White M, Pierce E, Tudoreanu E, Boeszoermenyi A, Shtridelman Y . The genetic code--more than just a table. Cell Biochem Biophys. 2009; 55(2):107-16. DOI: 10.1007/s12013-009-9060-9. View

Wilkie G, Dickson K, Gray N . Regulation of mRNA translation by 5'- and 3'-UTR-binding factors. Trends Biochem Sci. 2003; 28(4):182-8. DOI: 10.1016/S0968-0004(03)00051-3. View

Katz L, Burge C . Widespread selection for local RNA secondary structure in coding regions of bacterial genes. Genome Res. 2003; 13(9):2042-51. PMC: 403678. DOI: 10.1101/gr.1257503. View

Anderson C, Shen M, Eisenstein R, Leibold E . Mammalian iron metabolism and its control by iron regulatory proteins. Biochim Biophys Acta. 2012; 1823(9):1468-83. PMC: 3675657. DOI: 10.1016/j.bbamcr.2012.05.010. View

Jiang M, Anderson J, Gillespie J, Mayne M . uShuffle: a useful tool for shuffling biological sequences while preserving the k-let counts. BMC Bioinformatics. 2008; 9:192. PMC: 2375906. DOI: 10.1186/1471-2105-9-192. View

Soto I, Fontanesi F, Liu J, Barrientos A . Biogenesis and assembly of eukaryotic cytochrome c oxidase catalytic core. Biochim Biophys Acta. 2011; 1817(6):883-97. PMC: 3262112. DOI: 10.1016/j.bbabio.2011.09.005. View

FITCH W . The large extent of putative secondary nucleic acid structure in random nucleotide sequences or amino acid derived messenger-RNA. J Mol Evol. 1974; 3(4):279-91. DOI: 10.1007/BF01796043. View

Russu I, Ho N, Ho C . Role of the beta 146 histidyl residue in the alkaline Bohr effect of hemoglobin. Biochemistry. 1980; 19(5):1043-52. DOI: 10.1021/bi00546a033. View

10.

Wen J, Lancaster L, Hodges C, Zeri A, Yoshimura S, Noller H . Following translation by single ribosomes one codon at a time. Nature. 2008; 452(7187):598-603. PMC: 2556548. DOI: 10.1038/nature06716. View

11.

Bartenschlager R, Schaller H . A short cis-acting sequence is required for hepatitis B virus pregenome encapsidation and sufficient for packaging of foreign RNA. EMBO J. 1990; 9(10):3389-96. PMC: 552077. DOI: 10.1002/j.1460-2075.1990.tb07540.x. View

12.

Lorenz R, Bernhart S, Honer Zu Siederdissen C, Tafer H, Flamm C, Stadler P . ViennaRNA Package 2.0. Algorithms Mol Biol. 2011; 6:26. PMC: 3319429. DOI: 10.1186/1748-7188-6-26. View

13.

Allen J . Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression. Proc Natl Acad Sci U S A. 2015; 112(33):10231-8. PMC: 4547249. DOI: 10.1073/pnas.1500012112. View

14.

Zur H, Tuller T . Strong association between mRNA folding strength and protein abundance in S. cerevisiae. EMBO Rep. 2012; 13(3):272-7. PMC: 3323128. DOI: 10.1038/embor.2011.262. View

15.

Liu Y, Wimmer E, Paul A . Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim Biophys Acta. 2009; 1789(9-10):495-517. PMC: 2783963. DOI: 10.1016/j.bbagrm.2009.09.007. View

16.

Roseman M . Hydrophilicity of polar amino acid side-chains is markedly reduced by flanking peptide bonds. J Mol Biol. 1988; 200(3):513-22. DOI: 10.1016/0022-2836(88)90540-2. View

17.

Oresic M, Dehn M, Korenblum D, Shalloway D . Tracing specific synonymous codon-secondary structure correlations through evolution. J Mol Evol. 2003; 56(4):473-84. DOI: 10.1007/s00239-002-2418-x. View

18.

Gu W, Li M, Xu Y, Wang T, Ko J, Zhou T . The impact of RNA structure on coding sequence evolution in both bacteria and eukaryotes. BMC Evol Biol. 2014; 14:87. PMC: 4021280. DOI: 10.1186/1471-2148-14-87. View

19.

Miyata T, Miyazawa S, Yasunaga T . Two types of amino acid substitutions in protein evolution. J Mol Evol. 1979; 12(3):219-36. DOI: 10.1007/BF01732340. View

20.

Wirth C, Brandt U, Hunte C, Zickermann V . Structure and function of mitochondrial complex I. Biochim Biophys Acta. 2016; 1857(7):902-14. DOI: 10.1016/j.bbabio.2016.02.013. View