Distribution of mutational fitness effects and of epistasis in the 5' untranslated region of a plant RNA virus

BMC Evolutionary Biology

Volumn 15, Issue 1, 2015, Pages

  Bernet, Guillermo P ^a   Elena, Santiago F ^a,b  

^a CSIC   (Spain)

^b SANTA FE INSTITUTE   (United States)

Author keywords

Distribution of mutational fitness effects; Plant virus; Potyvirus; RNA folding; RNA regulatory sequences; Virus evolution

Indexed keywords

EPISTASIS; EVOLUTIONARY BIOLOGY; EVOLUTIONARY THEORY; FITNESS; GENE EXPRESSION; HOMEOSTASIS; MUTATION; PLANT; RNA; TOBACCO; VIRUS;

POTYVIRUS; RNA VIRUSES; TOBACCO ETCH VIRUS;

5' UNTRANSLATED REGION; VIRUS RNA;

5' UNTRANSLATED REGION; CHEMISTRY; EPISTASIS; EVOLUTION; GENETIC SELECTION; GENETICS; MUTATION; POTYVIRUS; RNA FOLDING;

5' UNTRANSLATED REGIONS; BIOLOGICAL EVOLUTION; EPISTASIS, GENETIC; MUTATION; POTYVIRUS; RNA FOLDING; RNA, VIRAL; SELECTION, GENETIC;

EID: 84952636503     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-015-0555-2     Document Type: Article

References (61)

1. Jacob F, Monod J. On the regulation of gene activity. Cold Spring Harb Symp Quant Biol. 1961;26:139-209.
2. Gale M, Tan SL, Katze MG. Translational control of viral gene expression in eukaryotes. Microbiol Mol Biol Rev. 2000;64:239-80.
3. Dimmock N, Easton A, Leppard K. Introduction to modern virology. 6th ed. Malden: Blackwell Publishing Ltd; 2007.
4. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell. 2009;136:731-45.
5. Firth AE, Brierley I. Non-canonical translation in RNA viruses. J Gen Virol. 2012;93:1385-409.
6. Kneller ELP, Rakotondrafara AM, Miller WA. Cap-independent translation of plant viral RNAs. Virus Res. 2006;119:63-75.
7. Hellendoorn K, Verlaan PW, Pleij CW. A functional role for the conserved protonatable hairpins in the 5' untranslated region of Turnip yellow mosaic virus RNA. J Virol. 1997;71:8774-9.
8. Van Marle G, Dobbe JC, Gultyaev AP, Luytjes W, Spaan WJ, Snijder EJ. Arterivirus discontinuous mRNA transcription is guided by base pairing between sense and antisense transcription-regulating sequences. Proc Natl Acad Sci USA. 1999;96:12056-61.
9. Friebe P, Lohmann V, Krieger N, Bartenschlager R. Sequences in the 5' nontranslated region of Hepatitis C virus required for RNA replication. J Virol. 2001;75:12047-57.
10. Luo G, Xin S, Cai Z. Role of the 5'-proximal stem-loop structure of the 5' untranslated region in replication and translation of Hepatitis C virus RNA. J Virol. 2003;77:3312-8.
11. Sasaki J, Taniguchi K. The 5'-end sequence of the genome of Aichi virus, a picornavirus, contains an element critical for viral RNA encapsidation. J Virol. 2003;77:3542-8.
12. Kwon SJ, Park MR, Kim KW, Plante CA, Hemenway CL, Kim KH. cis-Acting sequences required for coat protein binding and in vitro assembly of Potato virus X. Virology. 2005;334:83-97.
13. Hsu YH, Chen HC, Cheng J, Annamalai P, Lin BY, Wu CT, et al. Crucial role of the 5' conserved structure of Bamboo mosaic virus satellite RNA in downregulation of helper viral RNA replication. J Virol. 2006;80:2566-74.
14. Keightley PD. The distribution of mutation effects on viability in Drosophila melanogaster. Genetics. 1994;138:1315-22.
15. Keightley PD, Davies EK, Peters AD, Shaw RG. Properties of ethylmethane sulfonate-induced mutations affecting life-history traits in Caenorhabditis elegans and inferences about bivariate distributions of mutation effects. Genetics. 2000;156:143-54.
16. Shaw FH, Geyer CJ, Shaw RG. A comprehensive model of mutations affecting fitness and inferences for Arabidopsis thaliana. Evolution. 2002;56:453-63.
17. Elena SF, Moya A. Rate of deleterious mutation and the distribution of its effects on fitness in Vesicular stomatitis virus. J Evol Biol. 1999;12:1078-88.
18. Sanjuán R, Moya A, Elena SF. The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci USA. 2004;101:8396-401.
19. Carrasco P, de la Iglesia F, Elena SF. Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. J Virol. 2007;81:12979-84.
20. Peris JB, Davis P, Cuevas JM, Nebot MR, Sanjuán R. Distribution of fitness effects caused by single-nucleotide substitutions in bacteriophage f1. Genetics. 2010;185:603-9.
21. Dean AM, Thornton JW. Mechanistic approaches to the study of evolution: the functional synthesis. Nat Rev Genet. 2007;8:675-88.
22. Lalić J, Cuevas JM, Elena SF. Effect of host species on the distribution of mutational fitness effects for an RNA virus. PLoS Genet. 2011;7:e1002378.
23. Vale PF, Choisy M, Froissart R, Sanjuán R, Gandon S. The distribution of mutational fitness effects of phage φX174 on different hosts. Evolution. 2012;68:3495-507.
24. Elena SF, Carrasco P, Daròs JA, Sanjuán R. Mechanisms of genetic robustness in RNA viruses. EMBO Rep. 2006;7:168-73.
25. Eyre-Walker A, Keightley PD. The distribution of fitness effects of new mutations. Nat Rev Genet. 2007;8:610-8.
26. Sanjuán R. Mutational fitness effects in RNA and single-stranded DNA viruses: common patterns revealed by site-directed mutagenesis studies. Phil Trans R Soc B. 2010;365:1975-82.
27. Bataillon T, Bailey SF. Effects of new mutations on fitness: Insights from models and data. Ann NY Acad Sci. 2014;1320:76-92.
28. Sanjuán R, Moya A, Elena SF. The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA. 2004;101:15376-9.
29. Lalić J, Elena SF. Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus. Heredity. 2012;109:71-7.
30. Sanjuán R. Quantifying antagonistic epistasis in a multifunctional RNA secondary structure of the Rous sarcoma virus. J Gen Virol. 2006;87:1595-602.
31. Van Opijnen T, Boerlijst MC, Berkhout B. Effects of random mutations in the Human immunodeficiency virus type 1 transcriptional promoter on viral fitness in different host cell environments. J Virol. 2006;80:6678-85.
32. Urcuqui-Inchima S, Haenni AL, Bernardi F. Potyvirus proteins: a wealth of functions. Virus Res. 2001;74:157-75.
33. Chung BYW, Miller WA, Atkins JF, Firth AE. An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci USA. 2008;105:5897-902.
34. Gallie DR. Cap-independent translation conferred by the 5' leader of Tobacco etch virus is eukaryotic initiation factor 4G dependent. J Virol. 2001;75:12141-52.
35. Zeenko V, Gallie DR. Cap-independent translation of Tobacco etch virus is conferred by an RNA pseudoknot in the 5'-leader. J Biol Chem. 2005;280:26813-24.
36. Niepel M, Gallie DR. Identification and characterization of the functional elements within the Tobacco etch virus 5' leader required for cap-independent translation. J Virol. 1999;73:9080-8.
37. Kawarasaki Y, Kasahara S, Kodera N, Shinbata T, Sekiguchi S, Nakano H, et al. A trimmed viral cap-independent translation enhancing sequence for rapid in vitro gene expression. Biotechnol Prog. 2000;16:517-21.
38. Carrington JC, Freed DD. Cap-independent enhancement of translation by a plant potyvirus 5' nontranslated region. J Virol. 1990;64:1590-7.
39. Gallie DR, Tanguay RL, Leathers V. The tobacco etch viral 5' leader and poly(A) tail are functionally synergistic regulators of translation. Gene. 1995;165:233-8.
40. Shukla DD, Ward CW, Brunt AA. The Potyviridae. Wallingford: CAB International; 1994.
41. Bedoya LC, Daròs JA. Stability of Tobacco etch virus infectious clones in plasmid vectors. Virus Res. 2010;149:234-40.
42. Lorenz R, Bernhart SH, Höner Zu Siederdissen C, Tafer H, Flamm C, Stadler PF, et al. ViennaRNA Package 2.0. Algorithms Mol Biol. 2011;6:26.
43. Smith C, Heyne S, Richter AS, Will S, Backofen R. Freiburg RNA tools: a web server integrating IntaRNA, ExpaRNA and LocARNA. Nucl Acids Res. 2010;38:W373-7.
44. Sanjuán R, Forment J, Elena SF. In silico predicted robustness of viroids RNA secondary structures. I. The effect of single mutations. Mol Biol Evol. 2006;23:1427-36.
45. Wagner A, Stadler PF. Viral RNA and evolved mutational robustness. J Exp Zool. 1999;285:119-27.
46. Wilkinson KA, Merino EJ, Weeks KM. Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat Protoc. 2006;1:1610-6.
47. McGinnis JL, Duncan CDS, Weeks KM. High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleoprotein assembly. Meth Enzymol. 2009;468:67-89.
48. Karabiber F, McGinnis JL, Favorov OV, Weeks KM. QuShape: rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis. RNA. 2013;19:63-73.
49. Hajdin CE, Bellaousov S, Huggins W, Leonard CW, Mathews DH, Weeks KM. Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc Natl Acad Sci USA. 2013;110:5498-503.
50. Darty K, Denise A, Ponty Y. VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics. 2009;25:1974-5.
51. Carrasco P, Daròs JA, Agudelo-Romero P, Elena SF. A real-time RT-PCR assay for quantifying the fitness of Tobacco etch virus in competition experiments. J Virol Meth. 2007;139:181-8.
52. Kouyos RD, Silander OK, Bonhoeffer S. Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol Evol. 2007;6:308-15.
53. Poelwijk FJ, Tanase-Nicolas S, Kiviet DJ, Tans SJ. Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J Theor Biol. 2011;272:141-4.
54. Weinreich DM, Watson RA, Chao L. Perspective: sign epistasis and genetic constraints on evolutionary trajectories. Evolution. 2005;59:1165-74.
55. Emerson JJ, Li WH. The genetic basis of evolutionary change in gene expression levels. Phil Trans R Soc B. 2010;365:2581-90.
56. Gartield DA, Wray GA. The evolution of gene regulatory interactions. Bioscience. 2010;60:15-23.
57. Gallego Romero I, Rivinsky I, Gilad Y. Comparative studies of gene expression and the evolution of gene regulation. Nat Rev Genet. 2012;13:505-16.
58. Wilke CO, Lenski RE, Adami C. Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol. 2003;3:3.
59. Cowperthwaite MC, Bull JJ, Meyers LA. Distribution of beneficial fitness effects in RNA. Genetics. 2005;170:1449-57.
60. Manrubia SC, Sanjuán R. Shape matters: effect of point mutations on RNA secondary structure. Adv Complex Syst. 2013;16:1250052.
61. Elena SF, Solé RV, Sardanyés J. Simple genomes, complex interactions: epistasis in RNA virus. Chaos. 2010;20:026106.