Negative Epistasis in Experimental RNA Fitness Landscapes

Journal of Molecular Evolution

Volumn 85, Issue 5-6, 2017, Pages 159-168

  Bendixsen, Devin P ^a   Østman, Bjørn ^b,c   Hayden, Eric J ^a  

^a BOISE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epistasis; Evolution; Fitness landscapes; Mutations; ncRNA

Indexed keywords

RNA;

BIOLOGICAL MODEL; COMPUTER SIMULATION; EPISTASIS; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MUTATION; REPRODUCTIVE FITNESS; SACCHAROMYCES CEREVISIAE;

COMPUTER SIMULATION; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; GENETIC FITNESS; MODELS, GENETIC; MUTATION; RNA; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC;

EID: 85033477230     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-017-9817-5     Document Type: Review

References (54)

1. Bershtein S, Segal M, Bekerman R et al (2006) Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444:929–932. https://doi.org/10.1038/nature05385
2. Bloom JD, Arnold FH (2009) Colloquium papers: in the light of directed evolution: pathways of adaptive protein evolution. Proc Natl Acad Sci 106:9995–10000. https://doi.org/10.1073/pnas.0901522106
3. Bloom JD, Wilke CO, Arnold FH, Adami C (2004) Stability and the evolvability of function in a model protein. Biophys J 86:2758–2764. https://doi.org/10.1016/S0006-3495(04)74329-5
4. Bonhoeffer S, Chappey C, Parkin NT et al (2004) Evidence for positive epistasis in HIV-1. Science 306:1547–1550. https://doi.org/10.1126/science.1101786
5. Chakshusmathi G, Kim SD, Rubinson DA, Wolin SL (2003) A La protein requirement for efficient pre-tRNA folding. EMBO J 22:6562–6572. https://doi.org/10.1093/emboj/cdg625
6. Cherry JM, Hong EL, Amundsen C et al (2012) Saccharomyces genome database: the genomics resource of budding yeast. Nucleic Acids Res 40:D700–D705. https://doi.org/10.1093/nar/gkr1029
7. de la Iglesia F, Elena SF (2007) Fitness declines in tobacco etch virus upon serial bottleneck transfers. J Virol 81:4941–4947. https://doi.org/10.1128/JVI.02528-06
8. Desai MM, Fisher DS, Murray AW (2007) The speed of evolution and maintenance of variation in asexual populations. Curr Biol 17:385–394. https://doi.org/10.1016/j.cub.2007.01.072
9. Elena SF, Lenski RE (1997) Test of synergistic interactions among deleterious mutations in bacteria. Nature 390:395–398. https://doi.org/10.1038/37108
10. Eyre-Walker A, Keightley PD (2007) The distribution of fitness effects of new mutations. Nat Rev Genet 8:610–618. https://doi.org/10.1038/nrg2146
11. Fenster CB, Galloway LF, Chao L (1997) Epistasis and its consequences for the evolution of natural populations. Trends Ecol Evol 12:282–286
12. Halligan DL, Keightley PD (2009) Spontaneous mutation accumulation studies in evolutionary genetics. Annu Rev Ecol Evol Syst 40:151–172
13. Halls C, Mohr S, Del Campo M et al (2007) Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and-independent mechanisms, and general RNA chaperone activity. J Mol Biol 365:835–855
14. Hayden EJ, Riley CA, Burton AS, Lehman N (2005) RNA-directed construction of structurally complex and active ligase ribozymes through recombination. RNA 11:1678–1687. https://doi.org/10.1261/rna.2125305
15. Hayden EJ, Bendixsen DP, Wagner A (2015) Intramolecular phenotypic capacitance in a modular RNA molecule. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1420902112
16. He X, Qian W, Wang Z et al (2010) Prevalent positive epistasis in E. coli and S. cerevisiae metabolic networks. Nat Genet 42:272–276. https://doi.org/10.1038/ng.524
17. Herschlag D (1995) RNA chaperones and the RNA folding problem. J Biol Chem 270:20871–20874
18. Herschlag D, Khosla M, Tsuchihashi Z, Karpel RL (1994) An RNA chaperone activity of non-specific RNA binding proteins in hammerhead ribozyme catalysis. EMBO J 13:2913
19. Hunziker M, Barandun J, Petfalski E et al (2016) UtpA and UtpB chaperone nascent pre-ribosomal RNA and U3 snoRNA to initiate eukaryotic ribosome assembly. Nat Commun 7:12090. https://doi.org/10.1038/ncomms12090
20. Jarosz DF, Lindquist S (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330:1820–1824. https://doi.org/10.1126/science.1195487
21. Jiménez JI, Xulvi-Brunet R, Campbell GW et al (2013) Comprehensive experimental fitness landscape and evolutionary network for small RNA. Proc Natl Acad Sci 110:14984–14989. https://doi.org/10.1073/pnas.1307604110
22. Kobori S, Yokobayashi Y (2016) High-throughput mutational analysis of a twister ribozyme. Angew Chem Int Ed 55:10354–10357. https://doi.org/10.1002/anie.201605470
23. Kouyos RD, Silander OK, Bonhoeffer S (2007) Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol Evol 22:308–315
24. Kun A, Santos M, Szathmary E (2005) Real ribozymes suggest a relaxed error threshold. Nat Genet 37:1008–1011. https://doi.org/10.1038/ng1621
25. Lehman N (2003) A case for the extreme antiquity of recombination. J Mol Evol 56:770–777. https://doi.org/10.1007/s00239-003-2454-1
26. Li C, Qian W, Maclean CJ, Zhang J (2016) The fitness landscape of a tRNA gene. Science 352:837–840. https://doi.org/10.1126/science.aae0568
27. Maraia RJ, Arimbasseri AG (2017) Factors that shape eukaryotic tRNAomes: processing, modification and anticodon–codon use. Biomolecules 7:26. https://doi.org/10.3390/biom7010026
28. Meyers LA, Lee JF, Cowperthwaite M, Ellington AD (2004) The Robustness of naturally and artificially selected nucleic acid secondary structures. J Mol Evol 58:681–691. https://doi.org/10.1007/s00239-004-2590-2
29. Ostman B, Hintze A, Adami C (2012) Impact of epistasis and pleiotropy on evolutionary adaptation. Proc Biol Sci 279:247–256. https://doi.org/10.1098/rspb.2011.0870
30. Pesce D, Lehman N, de Visser JAGM (2016) Sex in a test tube: testing the benefits of in vitro recombination. Philos Trans R Soc Lond B Biol Sci. https://doi.org/10.1098/rstb.2015.0529
31. Puchta O, Cseke B, Czaja H et al (2016) Network of epistatic interactions within a yeast snoRNA. Science 352:840–844. https://doi.org/10.1126/science.aaf0965
32. Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624. https://doi.org/10.1038/nature749
33. Reinhold-Hurek B, Shub DA (1992) Self-splicing introns in tRNA genes of widely divergent bacteria. Nature 357:173–176. https://doi.org/10.1038/357173a0
34. Roth A, Weinberg Z, Chen AGY et al (2014) A widespread self-cleaving ribozyme class is revealed by bioinformatics. Nat Chem Biol 10:56–60. https://doi.org/10.1038/nchembio.1386
35. Rudan M, Schneider D, Warnecke T, Krisko A (2015) RNA chaperones buffer deleterious mutations in E. coli. eLife. https://doi.org/10.7554/eLife.04745
36. Russell R (2008) RNA misfolding and the action of chaperones. Front Biosci J Virtual Libr 13:1–20
37. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342. https://doi.org/10.1038/24550
38. Sailer ZR, Harms MJ (2017) Detecting high-order epistasis in nonlinear genotype-phenotype maps. Genetics 205:1079–1088. https://doi.org/10.1534/genetics.116.195214
39. Sanjuán R (2010) Mutational fitness effects in RNA and single-stranded DNA viruses: common patterns revealed by site-directed mutagenesis studies. Philos Trans R Soc Lond B Biol Sci 365:1975–1982. https://doi.org/10.1098/rstb.2010.0063
40. Sanjuán R, Moya A, Elena SF (2004) The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci USA 101:8396–8401. https://doi.org/10.1073/pnas.0400146101
41. Sinan S, Yuan X, Russell R (2011) The Azoarcus group I intron ribozyme misfolds and is accelerated for refolding by ATP-dependent RNA chaperone proteins. J Biol Chem 286:37304–37312
42. Soltanieh S, Osheim YN, Spasov K et al (2015) DEAD-box RNA helicase Dbp4 is required for small-subunit processome formation and function. Mol Cell Biol 35:816. https://doi.org/10.1128/MCB.01348-14
43. Soskine M, Tawfik DS (2010) Mutational effects and the evolution of new protein functions. Nat Rev Genet 11:572–582. https://doi.org/10.1038/nrg2808
44. Vaidya N, Manapat ML, Chen IA et al (2012) Spontaneous network formation among cooperative RNA replicators. Nature 491:72–77. https://doi.org/10.1038/nature11549
45. van Nimwegen E, Crutchfield JP, Huynen M (1999) Neutral evolution of mutational robustness. Proc Natl Acad Sci USA 96:9716–9720
46. Wagner A (2005) Robustness and evolvability in living systems. Princton University Press, Princeton
47. Wagner A (2011) The origins of evolutionary innovations: a theory of transformative change in living systems. OUP, Oxford
48. Weinreich DM, Watson RA, Chao L (2005) Perspective: Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165–1174
49. Weinreich DM, Lan Y, Wylie CS, Heckendorn RB (2013) Should evolutionary geneticists worry about higher-order epistasis? Curr Opin Genet Dev 23:700–707. https://doi.org/10.1016/j.gde.2013.10.007
50. Weissman DB, Desai MM, Fisher DS, Feldman MW (2009) The rate at which asexual populations cross fitness valleys. Theor Popul Biol 75:286–300. https://doi.org/10.1016/j.tpb.2009.02.006
51. Whitlock MC, Phillips PC, Moore FB-G, Tonsor SJ (1995) Multiple fitness peaks and epistasis. Annu Rev Ecol Syst 26:601–629. https://doi.org/10.1146/annurev.es.26.110195.003125
52. Wilke CO, Adami C (2001) Interaction between directional epistasis and average mutational effects. Proc Biol Sci 268:1469–1474. https://doi.org/10.1098/rspb.2001.1690
53. Wilke CO, Lenski RE, Adami C (2003) Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol 3:3
54. Wylie CS, Shakhnovich EI (2011) A biophysical protein folding model accounts for most mutational fitness effects in viruses. Proc Natl Acad Sci 108:9916–9921. https://doi.org/10.1073/pnas.1017572108