Selective constraints in conserved folded RNAs of drosophilid and hominid genomes

Molecular Biology and Evolution

Volumn 28, Issue 4, 2011, Pages 1519-1529

  Piskol, Robert ^a   Stephan, Wolfgang ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

RNA secondary structure; selection coefficients; selective constraints

Indexed keywords

UNTRANSLATED RNA;

ARTICLE; DROSOPHILA; EXON; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC SELECTION; GENETIC VARIABILITY; HOMINID; INTRON; NONHUMAN; PROTEIN SECONDARY STRUCTURE; RNA SPLICING; RNA STRUCTURE; SPECIES DIFFERENCE;

ANIMALS; BASE COMPOSITION; BIOLOGICAL EVOLUTION; CONSERVED SEQUENCE; DROSOPHILA; HOMINIDAE; HUMANS; NUCLEIC ACID CONFORMATION; RNA; SELECTION, GENETIC;

DROSOPHILIDAE; HOMINIDAE;

EID: 79952823671     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq343     Document Type: Article

References (65)

1. Amaral PP, Dinger ME, Mercer TR, Mattick JS. 2008. The eukaryotic genome as an RNA machine. Science 319(5871):1787-1789. (Pubitemid 351451554)
2. Amaral PP, Mattick JS. 2008. Noncoding RNA in development. Mamm Genome. 19(7-8):454-492.
3. Andolfatto P. 2001. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 18(3):279-290. (Pubitemid 32225077)
4. Bullock SL, Zicha D, Ish-Horowicz D. 2003. The Drosophila hairy RNA localization signal modulates the kinetics of cytoplasmic mRNA transport. EMBO J. 22(10):2484-2494. (Pubitemid 36604987)
5. Chen FC, Li WH. 2001. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet. 68(2):444-456.
6. Chen Y, Carlini DB, Baines JF, Parsch J, Braverman JM, Tanda S, Stephan W. 1999. RNA secondary structure and compensatory evolution. Genes Genet Syst. 74(6):271-286. (Pubitemid 30190884)
7. Chen Y, Stephan W. 2003. Compensatory evolution of a precursor messenger RNA secondary structure in the Drosophila melanogaster Adh gene. Proc Natl Acad Sci USA. 100(20):11499-11504. (Pubitemid 37205965)
8. Cutter AD. 2008. Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. Mol Biol Evol. 25(4):778-786. (Pubitemid 351398333)
9. Drosophila 12 Genomes Consortium. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203-219.
10. Duret L, Arndt PF. 2008. The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet. 4(5):e1000071.
11. Dutheil JY, Jossinet F, Westhof E. 2010. Base pairing constraints drive structural epistasis in ribosomal RNA sequences. Mol Biol Evol. 27(8):1868-1876.
12. Eory L, Halligan DL, Keightley PD. 2010. Distributions of selectively constrained sites and deleterious mutation rates in the hominid and murid genomes. Mol Biol Evol. 27(1):177-192.
13. Eperon LP, Graham IR, Griffiths AD, Eperon IC. 1988. Effects of RNA secondary structure on alternative splicing of pre-mRNA: is folding limited to a region behind the transcribing RNA polymerase? Cell 54(3):393-401.
14. Eyre-Walker A, Keightley PD. 2007. The distribution of fitness effects of new mutations. Nat Rev Genet. 8(8):610-618. (Pubitemid 47077280)
15. Eyre-Walker A, Woolfit M, Phelps T. 2006. The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173(2):891-900. (Pubitemid 43945904)
16. Farabaugh PJ. 1996. Programmed translational frameshifting. Annu Rev Genet. 30:507-528. (Pubitemid 27014476)
17. Gaffney DJ, Keightley PD. 2008. Effect of the assignment of ancestral CpG state on the estimation of nucleotide substitution rates in mammals. BMC Evol Biol. 8:265.
18. Gardner PP, Daub J, Tate JG, et al. (11 co-authors) 2009. Rfam: updates to the RNA families database. Nucleic Acids Res. 37:D136-D140.
19. Gott JM, Emeson RB. 2000. Functions and mechanisms of RNA editing. Annu Rev Genet. 34:499-531. (Pubitemid 32065931)
20. Griffiths-Jones S, Saini HK, Van Dongen S, Enright AJ. 2008. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36:D154-D158. (Pubitemid 351149713)
21. Halligan DL, Eyre-Walker A, Andolfatto P, Keightley PD. 2004. Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila. Genome Res. 14(2):273-279. (Pubitemid 38219840)
22. Halligan DL, Keightley PD. 2006. Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res. 16(7):875-884. (Pubitemid 43992911)
23. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P. 1994. Fast folding and comparison of RNA secondary structures. Monatshefte für Chemie 125:167-188.
24. Howe KJ, Ares M. 1997. Intron self-complementarity enforces exon inclusion in a yeast pre-mRNA. Proc Natl Acad Sci USA. 94(23):12467-12472. (Pubitemid 27492552)
25. Hutter S, Li H, Beisswanger S, de Lorenzo D, Stephan W. 2007. Distinctly different sex ratios in African and European populations of Drosophila melanogaster inferred from chromosomewide single nucleotide polymorphism data. Genetics 177(1):469-480. (Pubitemid 47555864)
26. Ichinose M, Iizuka M, Kado T, Takefu M. 2008. Compensatory evolution in diploid populations. Theor Popul Biol. 74(2):199-207.
27. Innan H, Stephan W. 2001. Selection intensity against deleterious mutations in RNA secondary structures and rate of compensatory nucleotide substitutions. Genetics 159(1):389-399. (Pubitemid 32917386)
28. Irion U, Johnston DS. 2007. bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445(7127):554-558. (Pubitemid 46197637)
29. John JCS, Facucho-Oliveira J, Jiang Y, Kelly R, Salah R. 2010. Mi-tochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Hum Reprod Update. 16(5): 488-509.
30. Keightley PD, Eyre-Walker A. 2007. Joint inference of the distribution of fitness effects of deleterious mutations and population demography based on nucleotide polymorphism frequencies. Genetics 177(4):2251-2261. (Pubitemid 350277004)
31. Keightley PD, Eyre-Walker A. 2010. What can we learn about the distribution of fitness effects of new mutations from DNA sequence data? Philos. Trans. R. Soc. B. 365(1544):1187-1193.
32. Keightley PD, Lercher MJ, Eyre-Walker A. 2005. Evidence for widespread degradation of gene control regions in hominid genomes. PLoS Biol. 3(2):e42.
33. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res. 12(6):996-1006. (Pubitemid 34662293)
34. Kimura M. 1980. Average time until fixation of a mutant allele in a finite population under continued mutation pressure: studies by analytical, numerical, and pseudo-sampling methods. Proc Natl Acad Sci USA. 77(1):522-526. (Pubitemid 10126069)
35. Kimura M. 1985. The role of compensatory neutral mutations in molecular evolution. J Genet. 64:7-19.
36. Kirby DA, Muse SV, Stephan W. 1995. Maintenance of pre-mRNA secondary structure by epistatic selection. Proc Natl Acad Sci USA. 92(20):9047-9051.
37. Kliman RM, Andolfatto P, Coyne JA, Depaulis F, Kreitman M, Berry AJ, McCarter J, Wakeley J, Hey J. 2000. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156(4):1913-1931. (Pubitemid 32001252)
38. Knies JL, Dang KK, Vision TJ, Hoffman NG, Swanstrom R, Burch CL. 2008. Compensatory evolution in RNA secondary structures increases substitution rate variation among sites. Mol Biol Evol. 25(8):1778-1787. (Pubitemid 352019863)
39. Koonin EV, Wolf YI. 2010. Constraints and plasticity in genome and molecular-phenome evolution. Nat Rev Genet. 11(7):487-498.
40. Leontis NB, Westhof E. 2001. Geometric nomenclature and classification of RNA base pairs. RNA. 7(4):499-512. (Pubitemid 32416808)
41. Li JB, Levanon EY, Yoon JK, Aach J, Xie B, Leproust E, Zhang K, Gao Y, Church GM. 2009. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324(5931):1210-1213.
42. MacDonald PM. 1990. bicoid mRNA localization signal: phylogenetic conservation of function and RNA secondary structure. Development 110(1):161-171. (Pubitemid 20287224)
43. Meer MV, Kondrashov AS, Artzy-Randrup Y, Kondrashov FA. 2010. Compensatory evolution in mitochondrial tRNAs navigates valleys of low fitness. Nature 464(7286):279-282.
44. Mimouni NK, Lyngsø RB, Griffiths-Jones S, Hein J. 2009. An analysis of structural influences on selection in RNA genes. Mol Biol Evol. 26(1)209-216.
45. Nachman MW, Crowell SL. 2000. Estimate of the mutation rate per nucleotide in humans. Genetics 156(1):297-304.
46. Namy O, Rousset JP, Napthine S, Brierley I. 2004. Reprogrammed genetic decoding in cellular gene expression. Mol Cell. 13(2):157-168. (Pubitemid 38183263)
47. Nasrallah CA, Mathews DH, Huelsenbeck JP. 2011. Quantifying the impact of dependent evolution among sites in phylogenetic inference. Syst Biol. 60(1):60-73.
48. Ohta T, Gillespie JH. 1996. Development of neutral and nearly neutral theories. Theor Popul Biol. 49(2):128-142.
49. Parmley JL, Urrutia AO, Potrzebowski L, Kaessmann H, Hurst LD. 2007. Splicing and the evolution of proteins in mammals. PLoS Biol. 5(2):e14.
50. Parsch J, Braverman JM, Stephan W. 2000. Comparative sequence analysis and patterns of covariation in RNA secondary structures. Genetics 154(2):909-921. (Pubitemid 30096609)
51. Parsch J, Novozhilov S, Saminadin-Peter SS, Wong KM, Andolfatto P. 2010. On the utility of short intron sequences as a reference for the detection of positive and negative selection in Drosophila. Mol Biol Evol. 27(6):1226-1234.
52. Parsons TJ, Muniec DS, Sullivan K, et al. (11 co-authors) 1997. A high observed substitutionrate in the human mitochondrial DNA control region. Nat Genet. 15(4):363-368. (Pubitemid 27147103)
53. Pedersen JS, Bejerano G, Siepel A, Rosenbloom K, Lindblad-Toh K, Lander ES, Kent J, Miller W, Haussler D. 2006. Identification and classification of conserved RNA secondary structures in the human genome. PLoS Comput Biol. 2(4):e33.
54. Piskol R, Stephan W. 2008. Analyzing the evolution of RNA secondary structures in vertebrate introns using Kimura's model of compensatory fitness interactions. Mol Biol Evol. 25(11):2483-2492.
55. Pozzoli U, Menozzi G, Fumagalli M, Cereda M, Comi GP, Cagliani R, Bresolin N, Sironi M. 2008. Both selective and neutral processes drive GC content evolution in the human genome. BMC Evol Biol. 8:99.
56. Savill NJ, Hoyle DC, Higgs PG. 2001. RNA sequence evolution with secondary structure constraints: comparison of substitution rate models using maximum-likelihood methods. Genetics 157(1):399-411. (Pubitemid 32066325)
57. Schug MD, Hutter CM, Wetterstrand KA, Gaudette MS, Mackay TF, Aquadro CF. 1998. The mutation rates of di-, tri- and tetranucleotide repeats in Drosophila melanogaster. Mol Biol Evol. 15(12):1751-1760. (Pubitemid 28550998)
58. Sorek R, Ast G. 2003. Intronic sequences flanking alternatively spliced exons are conserved between human and mouse. Genome Res. 13(7):1631-1637. (Pubitemid 36874480)
59. Stark A, Lin MF, Kheradpour P, et al. (46 co-authors) 2007. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450(7167):219-232. (Pubitemid 350100553)
60. Stephan W. 1996. The rate of compensatory evolution. Genetics 144(1):419-426. (Pubitemid 26291949)
61. Stephan W, Kirby DA. 1993. RNA folding in Drosophila shows a distance effect for compensatory fitness interactions. Genetics 135(1):97-103. (Pubitemid 23254060)
62. Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS. 2010. Non-coding RNAs: regulators of disease. J Pathol. 220(2):126-139.
63. Tavaré S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM, editor. Some Mathematical Questions in Biology: DNA Sequence Analysis (Lectures on Mathematics in the Life Sciences). Vol. 17. Providence (RI): American Mathematical Society. p. 57-86.
64. Tillier ER, Collins RA. 1998. High apparent rate of simultaneous compensatory base-pair substitutions in ribosomal RNA. Genetics 148(4):1993-2002. (Pubitemid 28180723)
65. Yang Z. 2007. Paml 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24(8):1586-1591. (Pubitemid 47236688)