Have a personal or library account? Click to login
Highly Similar Average Collateral Effect of Synonymous Mutations Across Alternative Reading Frames: A Potential Role In Evolvability Cover

Highly Similar Average Collateral Effect of Synonymous Mutations Across Alternative Reading Frames: A Potential Role In Evolvability

Open Access
|Mar 2023

References

  1. 1. Wichmann S, Ardern Z. Optimality in the standard genetic code is robust with respect to comparison code sets. Bio Systems. 2019 November;2019;185:104023. doi:10.10.1016/j.biosystems.2019.104023
  2. 2. Barrell BG, Air GM, Hutchison CA 3rd. Overlapping genes in bacteriophage phiX174. Nature. 1976;264(5581):34-41. doi:10.1038/264034a0
  3. 3. Firth AE, Brierley I. Non-canonical translation in RNA viruses. J Gen Virol. 2012;93(Pt 7):1385-1409. doi:10.1099/vir.0.042499-0
  4. 4. Cassan E, Arigon-Chifolleau AM, Mesnard JM, Gross A, Gascuel O. Concomitant emergence of the antisense protein gene of HIV-1 and of the pandemic. Proc Natl Acad Sci USA. 2016;113(41):11537-11542. doi:10.1073/pnas.1605739113
  5. 5. Affram Y, Zapata JC, Gholizadeh Z, Tolbert WD, Zhou W, Iglesias-Ussel MD, Pazgier M, Ray K, Latinovic OS, Romerio F. The HIV-1 antisense protein ASP is a transmembrane protein of the cell surface and an integral protein of the viral envelope. J Virol. 2019;93(21):e00574-19. doi:10.1128/JVI.00574-19
  6. 6. Nelson CW, Ardern Z, Goldberg TL, Meng C, Kuo CH, Ludwig C, Kolokotronis SO, Wei X. Dynamically evolving novel overlapping gene as a factor in the SARS-CoV-2 pandemic. Elife. 2020;9:e59633. doi:10.7554/eLife.59633
  7. 7. Firth AE. A putative new SARS-CoV protein, 3c, encoded in an ORF overlapping ORF3a. J Gen Virol. 2020;101(10):1085-1089. doi:10.1099/jgv.0.001469
  8. 8. Kreitmeier M, Ardern Z, Abele M, Ludwig C, Scherer S, Neuhaus K. Spotlight on alternative frame coding: Two long overlapping genes in Pseudomonas aeruginosa are translated and under purifying selection. iScience. 2022;25(2):103844. doi:10.1016/j.isci.2022.103844
  9. 9. Zehentner B, Ardern Z, Kreitmeier M, Scherer S, Neuhaus K. Evidence for numerous embedded antisense overlapping genes in diverse E. coli strains. bioRxiv. 2020. Available from: https://doi.org/10.1101/2020.11.18.388249
  10. 10. Ardern Z, Neuhaus K, Scherer S. Are Antisense Proteins in Prokaryotes Functional?. Front Mol Biosci. 2020;7:187. doi:10.3389/fmolb.2020.00187
  11. 11. Meydan S, Vázquez-Laslop N, Mankin Alexander S. Genes within genes in bacterial genomes. Microbiology Spectrum. 2018;6(4). Available from: https://doi.org/10.1128/microbiolspec.RWR-0020-2018
  12. 12. Hücker SM, Vanderhaeghen S, Abellan-Schneyder I, Scherer S, Neuhaus K. The novel anaerobiosis-responsive overlapping gene ano is overlapping antisense to the annotated gene ECs2385 of Escherichia coli O157:H7 Sakai. Front Microbiol. 2018;9:931. doi:10.3389/fmicb.2018.00931
  13. 13. Vanderhaeghen S, Zehentner B, Scherer S, Neuhaus K, Ardern Z. The novel EHEC gene asa overlaps the TEGT transporter gene in antisense and is regulated by NaCl and growth phase. Sci Rep. 2018;8(1):17875. doi:10.1038/s41598-018-35756-y
  14. 14. Gelsinger DR, Dallon E, Reddy R, Mohammad F, Buskirk AR, DiRuggiero J. Ribosome profiling in archaea reveals leaderless translation, novel translational initiation sites, and ribosome pausing at single codon resolution. Nucleic Acids Res. 2020;48(10):5201-5216. doi:10.1093/nar/gkaa304
  15. 15. Loughran G, Zhdanov AV, Mikhaylova MS, Andreev DE. Unusually efficient CUG initiation of an overlapping reading frame in POLG mRNA yields novel protein POLGARF. 2020;117(40):24936-24946. Available from: https://doi.org/10.1073/pnas.2001433117
  16. 16. Khan YA, Jungreis I, Wright JC, Mudge JM, Choudhary JS, Firth AE, Kellis M. Evidence for a novel overlapping coding sequence in POLG initiated at a CUG start codon. BMC Genet. 2020;21(1):25. doi:10.1186/s12863-020-0828-7
  17. 17. Mudge JM, Ruiz-Orera J, Prensner JR, Brunet MA, Gonzalez JM, Magrane M, Martinez T, Schulz JF, Yang YT, Alba MM, et al. A community-driven roadmap to advance research on translated open reading frames detected by Ribo-Seq. bioRxiv. 2021. Available from: https://doi.org/10.1101/2021.06.10.447896
  18. 18. Cao X, Khitun A, Luo Y, Na Z, Phoodokmai T, Sappakhaw K, Olatunji E, Uttamapinant C, Slavoff SA. Alt-RPL36 downregulates the PI3K-AKT-mTOR signaling pathway by interacting with TMEM24. Nat Commun. 2021;12(1):508. doi:10.1038/s41467-020-20841-6
  19. 19. Wright BW, Yi Z, Weissman JS, Chen J. The dark proteome: translation from noncanonical open reading frames. Trends Cell Biol. 2022;32(3):243-258. doi:10.1016/j.tcb.2021.10.010
  20. 20. Szekely M. Triple overlapping genes. Nature. 1978;272(5653): 492.
  21. 21. Siegel AF, Fitch WM. Degeneracy when DNA codes for overlapping genes. Mathematical Biosciences. 1980;49(1):1-16. Available from: https://doi.org/10.1016/0025-5564(80)90107-8
  22. 22. Smith TF, Waterman MS. Overlapping genes and information theory. J Theoret Biol. 1981;91(2):379-380.
  23. 23. Yockey HP. Rebuttal of ‘overlapping genes and information theory.’ J Theoret Biol. 1981;91(2):381-382.
  24. 24. Miyata T, Yasunaga T. Evolution of overlapping genes. Nature. 1978;272(5653):532-535.
  25. 25. Yockey HP. Do overlapping genes violate molecular biology and the theory of evolution? J Theoret Biol. 1979;80(1):21-26.
  26. 26. Kolata GB. Overlapping genes: more than anomalies? Science. 1977;196(4295):1187-1188.
  27. 27. Wright BW, Molloy MP, Jaschke PR. Overlapping genes in natural and engineered genomes. Nat Rev Genet. 2022;23(3): 154-168. doi:10.1038/s41576-021-00417-w
  28. 28. Brandes N, Linial M. Gene overlapping and size constraints in the viral world. Biol Direct. 2016 May;11:26.
  29. 29. Vakirlis N, Carvunis AR, McLysaght A. Synteny-based analyses indicate that sequence divergence is not the main source of orphan genes. Elife. 2020;9:e53500. doi:10.7554/eLife.53500
  30. 30. Keese PK, Gibbs A. Origins of genes: “big bang” or continuous creation?. Proc Natl Acad Sci USA. 1992;89(20):9489-9493. doi:10.1073/pnas.89.20.9489
  31. 31. Ohno S. Evolution by gene duplication. Berlin: Springer; 1970.
  32. 32. Carter CW. Simultaneous codon usage, the origin of the proteome, and the emergence of de-novo proteins. Cur Opin Struct Biol. 2021;68:142-148.
  33. 33. Watson AK, Lopez P, Bapteste E. Hundreds of out-of-frame remodeled gene families in the escherichia coli pangenome. Mol Biol Evol. 2022;39(1):msab329. Available from: https://doi.org/10.1093/molbev/msab329
  34. 34. Biba D, Klink G, Bazykin GA. Pairs of mutually compensatory frameshifting mutations contribute to protein evolution. Mol Biol Evol. 2022;39(3):msac031. Available from: https://doi.org/10.1093/molbev/msac031
  35. 35. Bartonek L, Braun D, Zagrovic B. Frameshifting preserves key physicochemical properties of proteins. Proc Natl Acad Sci USA. 2020;117(11):5907-5912.
  36. 36. Xu H, Zhang J. On the origin of frameshift-robustness of the standard genetic code. Mol Biol Evol. 2021a;38(10):4301-4309. doi:10.1093/molbev/msab1642021a
  37. 37. Blalock JE, Smith EM. Hydropathic anti-complementarity of amino acids based on the genetic code. Biochem Biophys Res Comm. 1984;121(1):203-207.
  38. 38. Zull JE, Smith SK. Is genetic code redundancy related to retention of structural information in both DNA strands? Trends Biochem Sci. 1990;15(7):257-261.
  39. 39. Konecny J, Eckert M, Schöniger M, Hofacker GL. Neutral adaptation of the genetic code to double-strand coding. J Mol Evol. 1993;36(5):407-416.
  40. 40. Blalock JE. Complementarity of peptides specified by ‘sense’ and ‘antisense’ strands of DNA. Trends Biotechnol. 1990;8(6): 140-144.
  41. 41. Willis S, Masel J. Gene birth contributes to structural disorder encoded by overlapping genes. genetics. 2018;210(1):303-313. doi:10.1534/genetics.118.301249
  42. 42. Wei X, Zhang J. A simple method for estimating the strength of natural selection on overlapping genes. Genome Biol Evol. 2015;7(10): 381-390. Available from: https://doi.org/10.1093/gbe/evu294
  43. 43. Osawa S. Evolution of the genetic code. Oxford: Oxford University Press; 1995.
  44. 44. Freeland SJ, Knight RD, Landweber LF, Hurst LD. Early fixation of an optimal genetic code. Mol Biol Evol. 2000;17(4):511-518. doi:10.1093/oxfordjournals.molbev.a026331
  45. 45. Freeland SJ, Hurst LD. The genetic code is one in a million. J Mol Evol. 1998;47(3):238-248.
  46. 46. Itzkovitz S, Alon U. The genetic code is nearly optimal for allowing additional information within protein-coding sequences. Genome Res. 2007;17(4):405-412.
  47. 47. Ilardo M, Meringer M, Freeland S, Rasulev B, Cleaves HJ 2nd. Extraordinarily adaptive properties of the genetically encoded amino acids. Sci Rep. 2015;5:9414. doi:10.1038/srep09414
  48. 48. Ilardo M, Bose R, Meringer M, Rasulev B, Grefenstette N, Stephenson J, Freeland S, Gillams RJ, Butch CJ, Cleaves HJ 3rd. Adaptive properties of the genetically encoded amino acid alphabet are inherited from its subsets. Sci Reports. 2019;9(12468). Available from: https://doi.org/10.1038/s41598-019-47574-x
  49. 49. Mayer-Bacon C, Freeland SJ. A broader context for understanding amino acid alphabet optimality. J Theo Biol. 2021 July;520:110661.
  50. 50. Freeland SJ. The Darwinian genetic code: An adaptation for adapting? Genet Program Evolvable Mach. 2002;3(2):113-127. Available from: https://doi.org/10.1023/A:1015527808424
  51. 51. Zhu W, Freeland SJ. The standard genetic code enhances adaptive evolution of proteins. J Theoret Biol. 2006;239(1):63-70.
  52. 52. Firnberg E, Ostermeier M. The genetic code constrains yet facilitates Darwinian evolution. Nucleic Acids Res. 2013;41(15): 7420-7428.
  53. 53. Tripathi S, Deem MW. The standard genetic code facilitates exploration of the space of functional nucleotide sequences. J Mol Evol. 2018;86(6):325-339.
  54. 54. Richter H, Engelbrecht A, editors. Recent advances in the theory and application of fitness landscapes. Berlin: Springer; 2014.
  55. 55. de Visser JA, Krug J. Empirical fitness landscapes and the predictability of evolution. Nat Rev Genet. 2014;15(7):480-490. doi:10.1038/nrg3744
  56. 56. Payne JL, Wagner A. The causes of evolvability and their evolution. Nat Rev Genet. 2019;20(1):24-38.
  57. 57. Chen JZ, Fowler DM, Tokuriki N. Environmental selection and epistasis in an empirical phenotype-environment-fitness landscape. Nat Ecol Evol. 2022;6(4):427-438. doi:10.1038/s41559-022-01675-5
  58. 58. Tenaillon O. The utility of Fisher’s geometric model in evolutionary genetics. Annu Rev Ecol Evol Syst. 2014;45:179-201. doi:10.1146/annurev-ecolsys-120213-091846
  59. 59. Fisher RA. The genetical theory of natural selection. Oxford: Clarendon Press; 1930. Available from: https://doi.org/10.5962/bhl.title.27468
  60. 60. Woese CR, Dugre DH, Dugre SA, Kondo M, Saxinger WC. On the fundamental nature and evolution of the genetic code. Cold Spring Harb Symp Quant Biol. 1966;31:723-736. doi:10.1101/sqb.1966.031.01.093
  61. 61. Buhrman H, van der Gulik PT, Kelk SM, Koolen WM, Stougie L. Some mathematical refinements concerning error minimization in the genetic code. IEEE/ACM Trans Comput Biol Bioinform. 2011;8(5):1358-1372. doi:10.1109/TCBB.2011.40
  62. 62. Lèbre S, Gascuel O. The combinatorics of overlapping genes. J Theoret Biol. 2017 February;415:90-101.
  63. 63. Shenhav L, Zeevi D. Resource conservation manifests in the genetic code. Science. 2020;370(6517): 683–687.
  64. 64. Rozhoňová H, Payne JL. Little evidence the standard genetic code is optimized for resource conservation. Mol Biol Evol. 2021;38(11):5127-5133.
  65. 65. Xu H, Zhang J. Is the genetic code optimized for resource conservation? Mol Biol Evol. 2021b;38(11):5122-5126.
  66. 66. Massey SE. A neutral origin for error minimization in the genetic code. J Mol Evol. 2008;67(5):510-516.
  67. 67. Massey SE. The neutral emergence of error minimized genetic codes superior to the standard genetic code. J Theoret Biol. 2016 November;408:237-242.
  68. 68. Di Giulio M. A non-neutral origin for error minimization in the origin of the genetic code. J Mol Evol. 2018;86(9):593-597.
  69. 69. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009;324(5924):218-223. doi:10.1126/science.1168978
  70. 70. Finkel Y, Mizrahi O, Nachshon A, Weingarten-Gabbay S, Morgenstern D, Yahalom-Ronen Y, Tamir H, Achdout H, Stein D, Israeli O, et al. The coding capacity of SARS-CoV-2. Nature. 2021;589(7840):125-130. doi:10.1038/s41586-020-2739-1
  71. 71. Firth AE. Mapping overlapping functional elements embedded within the protein-coding regions of RNA viruses. Nucleic Acids Res. 2014;42(20):12425-12439.
  72. 72. Sealfon RS, Lin MF, Jungreis I, Wolf MY, Kellis M, Sabeti PC. FRESCo: finding regions of excess synonymous constraint in diverse viruses. Genome Biol. 2015;16(1):38. doi:10.1186/s13059-015-0603-7
  73. 73. Schlub TE, Buchmann JP, Holmes EC. A simple method to detect candidate overlapping genes in viruses using single genome sequences. Mol Biol Evol. 2018;35(10):2572-2581.
  74. 74. Nelson CW, Ardern Z, Wei X. OLGenie: Estimating natural selection to predict functional overlapping genes. Mol Biol Evol. 2020;37(8):2440-2449. doi:10.1093/molbev/msaa087
  75. 75. Louis AA. Contingency, convergence and hyper-astronomical numbers in biological evolution. Stud Hist Philos Biol Biomed Sci. 2016;58:107-116. doi:10.1016/j.shpsc.2015.12.014
  76. 76. Keefe AD, Szostak JW. Functional proteins from a random-sequence library. Nature. 2001;410(6829):715-718.
  77. 77. Çakir U, Gabed N, Brunet M, Roucou X, Kryvoruchko I. Mosaic translation hypothesis: Chimeric polypeptides produced via multiple ribosomal frameshifting as a basis for adaptability [published online ahead of print, 2021 Nov 7]. FEBS J. 2021;10.1111/febs.16269. doi:10.1111/febs.16269
  78. 78. Kosinski LJ, Masel J. Readthrough errors purge deleterious cryptic sequences, facilitating the birth of coding sequences. Mol Biol Evol. 2020;37(6):1761-1774.
  79. 79. Fernandes JD, Faust TB, Strauli NB, Smith C, Crosby DC, Nakamura RL, Hernandez RD, Frankel AD. Functional segregation of overlapping genes in HIV. Cell. 2016;167(7):1762-1773. e12. doi:10.1016/j.cell.2016.11.031
  80. 80. Safari M, Jayaraman B, Yang S, Smith C, Fernandes JD, Frankel AD. Functional and structural segregation of overlapping helices in HIV-1. Elife. 2022;11:e72482. doi:10.7554/eLife.72482
  81. 81. Dingle K, Ghaddar F, Šulc P, Louis AA. Phenotype bias determines how natural RNA structures occupy the morphospace of all possible shapes. Mol Biol Evol. 2022;39(1):msab280. Available from: https://doi.org/10.1093/molbev/msab280.
  82. 82. Schulz L, Sendker FL, Hochberg GKA. Non-adaptive complexity and biochemical function. Curr Opin Structur Biol. 2022 April;73:102339.
  83. 83. Gould SJ, Lewontin RC. The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Concept Iss Evol Biol. 1979;205:79.
  84. 84. Morris SC. Life’s solution: Inevitable humans in a lonely universe. Cambridge: Cambridge University Press; 2003. Available from: https://doi.org/10.1017/CBO9780511535499
Language: English
Page range: 1 - 11
Published on: Mar 17, 2023
Published by: The Israel Biocomplexity Center
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2023 Stefan Wichmann, Zachary Ardern, published by The Israel Biocomplexity Center
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.