Natural selection drives rapid evolution of mouse embryonic heart enhancers

BMC Systems Biology

Volumn 6, Issue SUPPL.2, 2012, Pages

  Liao, Ben Yang ^a   Weng, Meng Pin ^a  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANIMAL EMBRYO; ARTICLE; ENHANCER REGION; GENE CONVERSION; GENETIC SELECTION; GENETICS; GENOMICS; HEART; METABOLISM; MOLECULAR EVOLUTION; MOUSE; PRENATAL DEVELOPMENT; TIME;

ANIMALS; EMBRYO, MAMMALIAN; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE CONVERSION; GENOMICS; HEART; MICE; SELECTION, GENETIC; TIME FACTORS;

MLCS; MLOWN;

EID: 84878652408     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-S2-S1     Document Type: Article

References (45)

1. Liao B-Y, Weng M-P, Zhang J. Contrasting genetic paths to morphological and physiological evolution. Proc Natl Acad Sci USA 2010, 107(16):7353-7358. 10.1073/pnas.0910339107, 2867737, 20368429.
2. Wray GA. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 2007, 8(3):206-216.
3. Carroll SB. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134(1):25-36. 10.1016/j.cell.2008.06.030, 18614008.
4. Ptashne M. Gene regulation by proteins acting nearby and at a distance. Nature 1986, 322(6081):697-701. 10.1038/322697a0, 3018583.
5. Dillon N, Sabbattini P. Functional gene expression domains: defining the functional unit of eukaryotic gene regulation. BioEssays 2000, 22(7):657-665. 10.1002/1521-1878(200007)22:7<657::AID-BIES8>3.0.CO;2-2, 10878578.
6. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, Minovitsky S, Dubchak I, Holt A, Lewis KD, et al. In vivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444(7118):499-502. 10.1038/nature05295, 17086198.
7. Borok MJ, Tran DA, Ho MCW, Drewell RA. Dissecting the regulatory switches of development: lessons from enhancer evolution in Drosophila. Development 2010, 137(1):5-13. 10.1242/dev.036160, 2796927, 20023155.
8. Robertson G, Hirst M, Bainbridge M, Bilenky M, Zhao Y, Zeng T, Euskirchen G, Bernier B, Varhol R, Delaney A, et al. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods 2007, 4(8):651-657. 10.1038/nmeth1068, 17558387.
9. Blow MJ, McCulley DJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, et al. ChIP-Seq identification of weakly conserved heart enhancers. Nat Genet 2010, 42(9):806-810. 10.1038/ng.650, 3138496, 20729851.
10. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457(7231):854-858. 10.1038/nature07730, 2745234, 19212405.
11. Hardison RC. Variable evolutionary signatures at the heart of enhancers. Nat Genet 2010, 42(9):734-735. 10.1038/ng0910-734, 20802475.
12. Frazer KA, Sheehan JB, Stokowski RP, Chen X, Hosseini R, Cheng JF, Fodor SP, Cox DR, Patil N. Evolutionarily conserved sequences on human chromosome 21. Genome Res 2001, 11(10):1651-1659. 10.1101/gr.198201, 311124, 11591642.
13. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 2005, 15(8):1034-1050. 10.1101/gr.3715005, 1182216, 16024819.
14. Jeffreys AJ, Royle NJ, Wilson V, Wong Z. Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable loci in human DNA. Nature 1988, 332(6161):278-281. 10.1038/332278a0, 3347271.
15. Duret L, Arndt PF. The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 2008, 4(5):e1000071. 10.1371/journal.pgen.1000071, 2346554, 18464896.
16. Hodgkinson A, Ladoukakis E, Eyre-Walker A. Cryptic variation in the human mutation rate. PLoS Biol 2009, 7(2):e1000027. 2634788, 19192947.
17. Tian D, Wang Q, Zhang P, Araki H, Yang S, Kreitman M, Nagylaki T, Hudson R, Bergelson J, Chen J-Q. Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes. Nature 2008, 455(7209):105-108. 10.1038/nature07175, 18641631.
18. Bird AP. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res 1980, 8(7):1499-1504. 10.1093/nar/8.7.1499, 324012, 6253938.
19. Vallender EJ, Lahn BT. Positive selection on the human genome. Hum Mol Genet 2004, 13(Spec No 2):R245-254.
20. Zhang J. Evolution of the human ASPM gene, a major determinant of brain size. Genetics 2003, 165(4):2063-2070. 1462882, 14704186.
21. Zhang J, He X. Significant impact of protein dispensability on the instantaneous rate of protein evolution. Mol Biol Evol 2005, 22(4):1147-1155. 10.1093/molbev/msi101, 15689524.
22. Liao B-Y, Scott NM, Zhang J. Impacts of gene essentiality, expression pattern, and gene compactness on the evolutionary rate of mammalian proteins. Mol Biol Evol 2006, 23(11):2072-2080. 10.1093/molbev/msl076, 16887903.
23. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 2002, 12(6):962-968. 1383730, 12045149.
24. Rocha EP, Danchin A. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol 2004, 21(1):108-116.
25. Julenius K, Pedersen AG. Protein evolution is faster outside the cell. Mol Biol Evol 2006, 23(11):2039-2048. 10.1093/molbev/msl081, 16891379.
26. Liao B-Y, Weng M-P, Zhang J. Impact of extracellularity on the evolutionary rate of mammalian proteins. Genome Biol Evol 2010, 2010:39-43. 2839354, 20333223.
27. Gu X, Su Z. Tissue-driven hypothesis of genomic evolution and sequence-expression correlations. Proc Natl Acad Sci USA 2007, 104(8):2779-2784. 10.1073/pnas.0610797104, 1815258, 17301236.
28. Tuller T, Kupiec M, Ruppin E. Evolutionary rate and gene expression across different brain regions. Genome Biol 2008, 9(9):R142. 10.1186/gb-2008-9-9-r142, 2592720, 18811952.
29. Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM, Chen CF, Thomas MA, Haussler D, Jacob HJ. Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 2004, 14(4):528-538. 10.1101/gr.1970304, 383296, 15059993.
30. Liao B-Y, Zhang J. Mouse duplicate genes are as essential as singletons. Trends Genet 2007, 23(8):378-381. 10.1016/j.tig.2007.05.006, 17559966.
31. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004, 101(16):6062-6067. 10.1073/pnas.0400782101, 395923, 15075390.
32. Hubbard TJ, Aken BL, Beal K, Ballester B, Caccamo M, Chen Y, Clarke L, Coates G, Cunningham F, Cutts T, et al. Ensembl 2007. Nucleic Acids Res 2007, 35(Database issue):D610-617. 1761443, 17148474.
33. Jukes TH, Cantor CR. Evolution of Protein Molecules. 1969, New York: Academic Press.
34. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591. 10.1093/molbev/msm088, 17483113.
35. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, et al. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 2008, 321(5891):956-960. 10.1126/science.1160342, 18599741.
36. Li W-H. Molecular Evolution. 1997, Sunderland, MA: Sinauer Associates.
37. Haygood R, Fedrigo O, Hanson B, Yokoyama K-D, Wray GA. Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet 2007, 39(9):1140-1144. 10.1038/ng2104, 17694055.
38. Blanchette M, Bataille AR, Chen X, Poitras C, Laganiere J, Lefebvre C, Deblois G, Giguere V, Ferretti V, Bergeron D, et al. Genome-wide computational prediction of transcriptional regulatory modules reveals new insights into human gene expression. Genome Res 2006, 16(5):656-668. 10.1101/gr.4866006, 1457048, 16606704.
39. Rooney AP, Zhang J. Rapid evolution of a primate sperm protein: relaxation of functional constraint or positive Darwinian selection?. Mol Biol Evol 1999, 16(5):706-710. 10.1093/oxfordjournals.molbev.a026153, 10335662.
40. Duret L, Galtier N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 2009, 10:285-311. 10.1146/annurev-genom-082908-150001, 19630562.
41. He X, Zhang J. Toward a molecular understanding of pleiotropy. Genetics 2006, 173(4):1885-1891. 10.1534/genetics.106.060269, 1569710, 16702416.
42. Zhang L, Li WH. Mammalian housekeeping genes evolve more slowly than tissue-specific genes. Mol Biol Evol 2004, 21(2):236-239.
43. Payseur BA, Nachman MW. Gene density and human nucleotide polymorphism. Mol Biol Evol 2002, 19(3):336-340. 10.1093/oxfordjournals.molbev.a004086, 11861892.
44. Xia Y, Franzosa EA, Gerstein MB. Integrated assessment of genomic correlates of protein evolutionary rate. PLoS Comput Biol 2009, 5(6):e1000413. 10.1371/journal.pcbi.1000413, 2688033, 19521505.
45. Versteeg R, van Schaik BD, van Batenburg MF, Roos M, Monajemi R, Caron H, Bussemaker HJ, van Kampen AH. The human transcriptome map reveals extremes in gene density, intron length, GC content, and repeat pattern for domains of highly and weakly expressed genes. Genome Res 2003, 13(9):1998-2004. 10.1101/gr.1649303, 403669, 12915492.