-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Pervasive Variation of Transcription Factor Orthologs Contributes to Regulatory Network Evolution
The phenotypic differences observed between closely related organisms are thought to be due largely to changes in regulatory networks. Changes in transcriptional networks can occur via mutations in cis binding sites, for which there are numerous known examples, as well as via binding specificity variation in transcription factors (TFs), a less studied phenomenon that has been observed primarily in multi-gene families. Though large-scale experimental studies ascertaining the extent to which TFs contribute to regulatory network variation across organisms are lacking and would be time-consuming, computational methods can begin to address this challenge. Here, we present a systematic, large-scale analysis of DNA-binding specificity evolution in TF orthologs by computationally leveraging specific features of Cys2-His2 zinc finger proteins, the largest class of TFs in animals and major components of their regulatory programs. We find not only that divergence of DNA-binding residues in 1-to-1 orthologous C2H2-ZFs is pervasive but also that these changes show evidence of functional constraint and occur in a gradual, evolutionarily viable manner. We conclude that the diversification of orthologous TFs has most likely played a major and largely unstudied role in gene regulatory network evolution in metazoans.
Vyšlo v časopise: Pervasive Variation of Transcription Factor Orthologs Contributes to Regulatory Network Evolution. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005011
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005011Souhrn
The phenotypic differences observed between closely related organisms are thought to be due largely to changes in regulatory networks. Changes in transcriptional networks can occur via mutations in cis binding sites, for which there are numerous known examples, as well as via binding specificity variation in transcription factors (TFs), a less studied phenomenon that has been observed primarily in multi-gene families. Though large-scale experimental studies ascertaining the extent to which TFs contribute to regulatory network variation across organisms are lacking and would be time-consuming, computational methods can begin to address this challenge. Here, we present a systematic, large-scale analysis of DNA-binding specificity evolution in TF orthologs by computationally leveraging specific features of Cys2-His2 zinc finger proteins, the largest class of TFs in animals and major components of their regulatory programs. We find not only that divergence of DNA-binding residues in 1-to-1 orthologous C2H2-ZFs is pervasive but also that these changes show evidence of functional constraint and occur in a gradual, evolutionarily viable manner. We conclude that the diversification of orthologous TFs has most likely played a major and largely unstudied role in gene regulatory network evolution in metazoans.
Zdroje
1. King M, Wilson A (1975) Evolution at two levels in humans and chimpanzees. Science 188 : 107–116. doi: 10.1126/science.1090005 1090005
2. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, et al. (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20 : 1377–1419. doi: 10.1093/molbev/msg140 12777501
3. Prud’homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. PNAS 104 : 8605–8612. doi: 10.1073/pnas.0700488104 17494759
4. Stern DL, Orgogozo V (2008) The loci of evolution: How predictable is genetic evolution? Evolution 62 : 2155–2177. doi: 10.1111/j.1558-5646.2008.00450.x 18616572
5. Liao BY, Weng MP, Zhang J (2010) Contrasting genetic paths to morphological and physiological evolution. PNAS 107 : 7353–7358. doi: 10.1073/pnas.0910339107 20368429
6. Britten RJ, Davidson EH (1969) Gene regulation for higher cells: A theory. Science 165 : 349–357. doi: 10.1126/science.165.3891.349 5789433
7. Stern DL (2000) Perspective: Evolutionary developmental biology and the problem of variation. Evolution 54 : 1079–1091. doi: 10.1554/0014-3820(2000)054%5B1079:PEDBAT%5D2.0.CO;2 11005278
8. Carroll SB (2005) Evolution at two levels: On genes and form. PLoS Biol 3: e245. doi: 10.1371/journal.pbio.0030245 16000021
9. Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8 : 206–216. doi: 10.1038/nrg2063 17304246
10. Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R, et al. (2014) Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343 : 780–783. doi: 10.1126/science.1248384 24531971
11. Wagner GP, Lynch VJ (2008) The gene regulatory logic of transcription factor evolution. Trends Ecol Evol 23 : 377–385. doi: 10.1016/j.tree.2008.03.006 18501470
12. Singh LN, Hannenhalli S (2008) Functional diversification of paralogous transcription factors via divergence in DNA binding site motif and in expression. PLoS ONE 3: e2345. doi: 10.1371/journal.pone.0002345 18523562
13. Emerson RO, Thomas JH (2009) Adaptive evolution in zinc finger transcription factors. PLoS Genet 5: e1000325. doi: 10.1371/journal.pgen.1000325 19119423
14. Baker CR, Tuch BB, Johnson AD (2011) Extensive DNA-binding specificity divergence of a conserved transcription regulator. PNAS 108 : 7493–7498. doi: 10.1073/pnas.1019177108 21498688
15. Nakagawa S, Gisselbrecht SS, Rogers JM, Hartl DL, Bulyk ML (2013) DNA-binding specificity changes in the evolution of forkhead transcription factors. PNAS 110 : 12349–12354. doi: 10.1073/pnas.1310430110 23836653
16. Sayou C, Monniaux M, Nanao MH, Moyroud E, Brockington SF, et al. (2014) A promiscuous intermediate underlies the evolution of LEAFY DNA-binding specificity. Science 343 : 645–648. doi: 10.1126/science.1248229 24436181
17. Galant R, Carroll SB (2002) Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415 : 910–913. doi: 10.1038/nature717 11859369
18. Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415 : 914–917. doi: 10.1038/nature716 11859370
19. Pabo CO, Peisach E, Grant RA (2001) Design and selection of novel Cys2His2 zinc finger proteins. Ann Rev Biochem 70 : 313–340. doi: 10.1146/annurev.biochem.70.1.313 11395410
20. Vaquerizas JM, Kummerfeld SK, Teichmann SA, Luscombe NM (2009) A census of human transcription factors: Function, expression and evolution. Nat Rev Genet 10 : 252–263. doi: 10.1038/nrg2538 19274049
21. Enuameh MS, Asriyan Y, Richards A, Christensen RG, Hall VL, et al. (2013) Global analysis of Drosophila Cys2-His2 zinc finger proteins reveals a multitude of novel recognition motifs and binding determinants. Genome Res 23 : 928–940. doi: 10.1101/gr.151472.112 23471540
22. Benos PV, Lapedes AS, Stormo GD (2002) Probabilistic code for DNA recognition by proteins of the EGR family. J Mol Biol 323 : 701–727. doi: 10.1016/S0022-2836(02)00917-8 12419259
23. Kaplan T, Friedman N, Margalit H (2005) Ab initio prediction of transcription factor targets using structural knowledge. PLoS Comput Biol 1: e1. doi: 10.1371/journal.pcbi.0010001 16103898
24. Persikov AV, Singh M (2014) De novo prediction of DNA-binding specificities for Cys2His2 zinc finger proteins. Nucleic Acids Res 42 : 97–108. doi: 10.1093/nar/gkt890 24097433
25. Gupta A, Christensen RG, Bell HA, Goodwin M, Patel RY, et al. (2014) An improved predictive recognition model for Cys2-His2 zinc finger proteins. Nucleic Acids Res 42 : 4800–4812. doi: 10.1093/nar/gku132 24523353
26. Persikov AV, Wetzel JL, Rowland EF, Oakes BL, Xu DJ, et al. (2015) A systematic survey of the Cys2His2 zinc finger DNA-binding landscape. Nucleic Acids Res In press: doi: 10.1093/nar/gku1395 25593323
27. Nowick K, Fields C, Gernat T, Caetano-Anolles D, Kholina N, et al. (2011) Gain, loss and divergence in primate zinc-finger genes: A rich resource for evolution of gene regulatory differences between species. PLoS ONE 6: e21553. doi: 10.1371/journal.pone.0021553 21738707
28. Shannon M, Hamilton AT, Gordon L, Branscomb E, Stubbs L (2003) Differential expansion of zinc-finger transcription factor loci in homologous human and mouse gene clusters. Genome Res 13 : 1097–1110. doi: 10.1101/gr.963903 12743021
29. Nowick K, Hamilton AT, Zhang H, Stubbs L (2010) Rapid sequence and expression divergence suggest selection for novel function in primate-specific KRAB-ZNF genes. Mol Biol Evol 27 : 2606–2617. doi: 10.1093/molbev/msq157 20573777
30. Stubbs L, Sun Y, Caetano-Anolles D (2011) Function and evolution of C2H2 zinc finger arrays, Houten, Netherlands: Springer Publishing. In A Handbook of Transcription Factors (ed. Hughes TR), pp. 75–94.
31. Liu H, Chang LH, Sun Y, Lu X, Stubbs L (2014) Deep vertebrate roots for mammalian zinc finger transcription factor subfamilies. Genome Biol Evol 6 : 510–525. doi: 10.1093/gbe/evu030 24534434
32. Looman C, Åbrink M, Mark C, Hellman L (2002) KRAB zinc finger proteins: An analysis of the molecular mechanisms governing their increase in numbers and complexity during evolution. Mol Biol Evol 19 : 2118–2130. doi: 10.1093/oxfordjournals.molbev.a004037 12446804
33. Knight R, Shimeld S (2001) Identification of conserved C2H2 zinc-finger gene families in the Bilateria. Genome Biol 2: R16.1–R16.8. doi: 10.1186/gb-2001-2-5-research0016
34. Seetharam A, Bai Y, Stuart G (2010) A survey of well conserved families of C2H2 zinc-finger genes in Daphnia. BMC Genomics 11 : 276–295. doi: 10.1186/1471-2164-11-276 20433734
35. Seetharam A, Stuart GW (2013) A study on the distribution of 37 well conserved families of C2H2 zinc finger genes in eukaryotes. BMC Genomics 14 : 420–426. doi: 10.1186/1471-2164-14-420 23800006
36. Oliver PL, Goodstadt L, Bayes JJ, Birtle Z, Roach KC, et al. (2009) Accelerated evolution of the PRDM9 speciation gene across diverse metazoan taxa. PLoS Genet 5: e1000753. doi: 10.1371/journal.pgen.1000753 19997497
37. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, et al. (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327 : 876–879. doi: 10.1126/science.1182363 20044541
38. Berg IL, Neumann R, Sarbajna S, Odenthal-Hesse L, Butler NJ, et al. (2011) Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations. PNAS 108 : 12378–12383. doi: 10.1073/pnas.1109531108 21750151
39. Ségurel L, Leffler EM, Przeworski M (2011) The case of the fickle fingers: How the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans. PLoS Biol 9: e1001211. doi: 10.1371/journal.pbio.1001211 22162947
40. Groeneveld LF, Atencia R, Garriga RM, Vigilant L (2012) High diversity at PRDM9 in chimpanzees and bonobos. PLoS ONE 7: e39064. doi: 10.1371/journal.pone.0039064 22768294
41. Hoekstra HE, Coyne JA (2007) The locus of evolution: Evo devo and the genetics of adaptation. Evolution 61 : 995–1016. doi: 10.1111/j.1558-5646.2007.00105.x 17492956
42. Drosophila 12 Genomes Consortium (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450 : 203–218. doi: 10.1038/nature06341 17994087
43. Marygold SJ, Leyland PC, Seal RL, Goodman JL, Thurmond J, et al. (2013) FlyBase: Improvements to the bibliography. Nucleic Acids Res 41 : 751–757. doi: 10.1093/nar/gks1024
44. Gompel N, Carroll SB (2003) Genetic mechanisms and constraints governing the evolution of correlated traits in Drosophilid flies. Nature 424 : 931–935. doi: 10.1038/nature01787 12931186
45. Jeong S, Rokas A, Carroll SB (2006) Regulation of body pigmentation by the Abdominal-B Hox protein and its gain and loss in Drosophila evolution. Cell 125 : 1387–1399. doi: 10.1016/j.cell.2006.04.043 16814723
46. Markow TA, O’Grady PM (2007) Drosophila biology in the genomic age. Genetics 177 : 1269–1276. doi: 10.1534/genetics.107.074112 18039866
47. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40 : 290–301. doi: 10.1093/nar/gkr1065
48. Finn RD, Clements J, Eddy SR (2011) HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res 39: W29–W37. doi: 10.1093/nar/gkr367 21593126
49. Meyer LR, Zweig AS, Hinrichs AS, Karolchik D, Kuhn RM, et al. (2013) The UCSC Genome Browser database: Extensions and updates 2013. Nucleic Acids Res 41 : 64–69. doi: 10.1093/nar/gks1048
50. Iuchi S (2001) Three classes of C2H2 zinc finger proteins. Cell Mol Life Sci 58 : 625–635. 11361095
51. Adryan B, Teichmann SA (2006) Flytf: A systematic review of site-specific transcription factors in the fruit fly Drosophila melanogaster. Bioinformatics 22 : 1532–1533. doi: 10.1093/bioinformatics/btl143 16613907
52. Wolfe SA, Nekludova L, Pabo CO (2000) DNA recognition by Cys2His2 zinc finger proteins. Ann Rev Bioph Biom 29 : 183–212. doi: 10.1146/annurev.biophys.29.1.183
53. Persikov AV, Singh M (2011) An expanded binding model for Cys2 His2 zinc finger protein-DNA interfaces. Phys Biol 8: e035010. doi: 10.1088/1478-3975/8/3/035010
54. Siggers T, Reddy J, Barron B, Bulyk ML (2014) Diversification of transcription factor paralogs via noncanonical modularity in C2H2 zinc finger DNA binding. Mol Cell 55 : 1–9. doi: 10.1016/j.molcel.2014.06.019
55. Mayrose I, Graur D, Ben-Tal N, Pupko T (2004) Comparison of site-specific rate-inference methods for protein sequences: Empirical Bayesian methods are superior. Mol Biol Evol 21 : 1781–1791. doi: 10.1093/molbev/msh194 15201400
56. Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267 : 275–276. doi: 10.1038/267275a0 865622
57. Yang Z (1997) PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 : 555–556. 9367129
58. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 : 652–654. doi: 10.1038/351652a0 1904993
59. Pool JE, Corbett-Detig RB, Sugino RP, Stevens KA, Cardeno CM, et al. (2012) Population genomics of sub-Saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet 8: e1003080. doi: 10.1371/journal.pgen.1003080 23284287
60. Bustamante CD, Wakeley J, Sawyer S, Hartl DL (2001) Directional selection and the site-frequency spectrum. Genetics 159 : 1779–1788. 11779814
61. Persikov AV, Rowland EF, Oakes BL, Singh M, Noyes MB (2014) Deep sequencing of large library selections allows computational discovery of diverse sets of zinc fingers that bind common targets. Nucleic Acids Res 42 : 1497–1508. doi: 10.1093/nar/gkt1034 24214968
62. Persikov AV, Osada R, Singh M (2009) Predicting DNA recognition by Cys2His2 zinc finger proteins. Bioinformatics 25 : 22–29. doi: 10.1093/bioinformatics/btn580 19008249
63. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14 : 1188–1190. doi: 10.1101/gr.849004 15173120
64. modENCODE Consortium (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330 : 1787–1797. doi: 10.1126/science.1198374 21177974
65. Zhu LJ, Christensen RG, Kazemian M, Hull CJ, Enuameh MS, et al. (2011) FlyFactorSurvey: A database of Drosophila transcription factor binding specificities determined using the bacterial one-hybrid system. Nucleic Acids Res 39: D111–D117. doi: 10.1093/nar/gkq858 21097781
66. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, et al. (2014) JASPAR 2014: An extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res 42: D142–D147. doi: 10.1093/nar/gkt997 24194598
67. Matys V, Fricke E, Geffers R, Gößling E, Haubrock M, et al. (2003) TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31 : 374–378. doi: 10.1093/nar/gkg108 12520026
68. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME Suite: Tools for motif discovery and searching. Nucleic Acids Res 37: W202–W208. doi: 10.1093/nar/gkp335 19458158
69. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, et al. (2004) GO∷TermFinder—open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20 : 3710–3715. doi: 10.1093/bioinformatics/bth456 15297299
70. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, et al. (2013) STRING v9.1: Protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41: D808–D815. doi: 10.1093/nar/gks1094 23203871
71. Li H, Baker B (1998) Her, a gene required for sexual differentiation in Drosophila, encodes a zinc finger protein with characteristics of ZFY-like proteins and is expressed independently of the sex determination hierarchy. Development 125 : 225–235. 9486796
72. Perezgasga L, Jiang J, Bolival B, Hiller M, Benson E, et al. (2004) Regulation of transcription of meiotic cell cycle and terminal differentiation genes by the testis-specific Zn-finger protein matotopetli. Development 131 : 1691–1702. doi: 10.1242/dev.01032 15084455
73. Laugier E, Yang Z, Fasano L, Kerridge S, Vola C (2005) A critical role of teashirt for patterning the ventral epidermis is masked by ectopic expression of tiptop, a paralog of teashirt in Drosophila. Dev Biol 283 : 446–458. doi: 10.1016/j.ydbio.2005.05.005 15936749
74. Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, et al. (2012) InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 40: D306–D312. doi: 10.1093/nar/gkr948 22096229
75. Chung HR, Schäfer U, Jäckle H, Böhm S (2002) Genomic expansion and clustering of ZAD-containing C2H2 zinc-finger genes in Drosophila. EMBO reports 3 : 1158–1162. doi: 10.1093/embo-reports/kvf243 12446571
76. Jauch R, Bourenkov GP, Chung HR, Urlaub H, Reidt U, et al. (2003) The zinc finger-associated domain of the Drosophila transcription factor Grauzone is a novel zinc-coordinating protein-protein interaction module. Structure 11 : 1393–1402. doi: 10.1016/j.str.2003.09.015 14604529
77. Chung HR, Löhr U, Jäckle H (2007) Lineage-specific expansion of the zinc finger associated domain ZAD. Mol Biol Evol 24 : 1934–1943. doi: 10.1093/molbev/msm121 17569752
78. Robinson SW, Herzyk P, Dow JAT, Leader DP (2013) FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster. Nucleic Acids Res 41: D744–D750. doi: 10.1093/nar/gks1141 23203866
79. Tuch BB, Galgoczy DJ, Hernday AD, Li H, Johnson AD (2008) The evolution of combinatorial gene regulation in fungi. PLoS Biol 6: e38. doi: 10.1371/journal.pbio.0060038 18303948
80. Borneman AR, Gianoulis TA, Zhang ZD, Yu H, Rozowsky J, et al. (2007) Divergence of transcription factor binding sites across related yeast species. Science 317 : 815–819. doi: 10.1126/science.1140748 17690298
81. Bradley RK, Li XY, Trapnell C, Davidson S, Pachter L, et al. (2010) Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 8: e1000343. doi: 10.1371/journal.pbio.1000343 20351773
82. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, et al. (2007) Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 39 : 730–732. doi: 10.1038/ng2047 17529977
83. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, et al. (2010) Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328 : 1036–1040. doi: 10.1126/science.1186176 20378774
84. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, et al. (2010) Variation in transcription factor binding among humans. Science 328 : 232–235. doi: 10.1126/science.1183621 20299548
85. Zheng W, Zhao H, Mancera E, Steinmetz LM, Snyder M (2010) Genetic analysis of variation in transcription factor binding in yeast. Nature 464 : 1187–1191. doi: 10.1038/nature08934 20237471
86. Pelham HRB, Brown DD (1980) A specific transcription factor that can bind either the 5S RNA gene or 5S RNA. PNAS 77 : 4170–4174. doi: 10.1073/pnas.77.7.4170 7001457
87. Brayer KJ, Segal DJ (2008) Keep your fingers off my DNA: Protein—protein interactions mediated by C2H2 zinc finger domains. Cell Biochem Biophys 50 : 111–131. doi: 10.1007/s12013-008-9008-5 18253864
88. Dermitzakis ET, Clark AG (2002) Evolution of transcription factor binding sites in mammalian gene regulatory regions: Conservation and turnover. Mol Biol Evol 19 : 1114–1121. doi: 10.1093/oxfordjournals.molbev.a004169 12082130
89. Costas J, Casares F, Vieira J (2003) Turnover of binding sites for transcription factors involved in early Drosophila development. Gene 310 : 215–220. doi: 10.1016/S0378-1119(03)00556-0 12801649
90. Moses AM, Pollard DA, Nix DA, Iyer VN, Li XY, et al. (2006) Large-scale turnover of functional transcription factor binding sites in Drosophila. PLoS Comput Biol 2: e130. doi: 10.1371/journal.pcbi.0020130 17040121
91. Doniger SW, Fay JC (2007) Frequent gain and loss of functional transcription factor binding sites. PLoS Comput Biol 3: e99. doi: 10.1371/journal.pcbi.0030099 17530920
92. Kim J, He X, Sinha S (2009) Evolution of regulatory sequences in 12 Drosophila species. PLoS Genet 5: e1000330. doi: 10.1371/journal.pgen.1000330 19132088
93. Venkataram S, Fay JC (2010) Is transcription factor binding site turnover a sufficient explanation for cis-regulatory sequence divergence? Genome Biol Evol 2 : 851–858. doi: 10.1093/gbe/evq066 21068212
94. Weirauch MT, Hughes TR (2010) Conserved expression without conserved regulatory sequence: The more things change, the more they stay the same. Trends Genet 26 : 66–74. doi: 10.1016/j.tig.2009.12.002 20083321
95. Tan K, Feizi H, Luo C, Fan SH, Ravasi T, et al. (2008) A systems approach to delineate functions of paralogous transcription factors: Role of the Yap family in the DNA damage response. PNAS 105 : 2934–2939. doi: 10.1073/pnas.0708670105 18287073
96. Lespinet O, Wolf YI, Koonin EV, Aravind L (2002) The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12 : 1048–1059. doi: 10.1101/gr.174302 12097341
97. Hamilton AT, Huntley S, Kim J, Branscomb E, Stubbs L (2003) Lineage-specific expansion of KRAB zinc-finger transcription factor genes: Implications for the evolution of vertebrate regulatory networks. CSHL Symposia on Quant Biol 68 : 131–140. doi: 10.1101/sqb.2003.68.131
98. Urrutia R (2003) KRAB-containing zinc-finger repressor proteins. Genome Biol 4 : 231. doi: 10.1186/gb-2003-4-10-231 14519192
99. Taylor JS, Raes J (2004) Duplication and divergence: The evolution of new genes and old ideas. Annu Rev Genet 38 : 615–643. doi: 10.1146/annurev.genet.38.072902.092831 15568988
100. Brunkard JO, Runkel AM, Zambryski PC (2015) Comment on “A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity.” Science 347 : 621. doi: 10.1126/science.1256011 25657240
101. Brockington SF, Moyroud E, Sayou C, Monniaux M, Nanao MH, et al. (2015) Response to Comment on “A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity.” Science 347 : 621. doi: 10.1126/science.1256011 25657241
102. Hu TT, Eisen MB, Thornton KR, Andolfatto P (2013) A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res 23 : 89–98. doi: 10.1101/gr.141689.112 22936249
103. Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7: e1002195. doi: 10.1371/journal.pcbi.1002195 22039361
104. Kent WJ (2002) Blat-the BLAST-Like Alignment Tool. Genome Res 12 : 656–664. doi: 10.1101/gr.229202 11932250
105. Notredame C, Higgins DG, Heringa J (2000) T-coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302 : 205–217. doi: 10.1006/jmbi.2000.4042 10964570
106. Vernot B, Stolzer M, Goldman A, Durand D (2008) Reconciliation with non-binary species trees. J Comput Biol 15 : 981–1006. doi: 10.1089/cmb.2008.0092 18808330
107. Kheradpour P, Stark A, Roy S, Kellis M (2007) Reliable prediction of regulator targets using 12 Drosophila genomes. Genome Res 17 : 1919–1931. doi: 10.1101/gr.7090407 17989251
108. Jiang P, Singh M (2014) CCAT: Combinatorial Code Analysis Tool for transcriptional regulation. Nucleic Acids Res 42 : 2833–2847. doi: 10.1093/nar/gkt1302 24366875
Štítky
Genetika Reprodukčná medicína
Článek NLRC5 Exclusively Transactivates MHC Class I and Related Genes through a Distinctive SXY ModuleČlánek Inhibition of Telomere Recombination by Inactivation of KEOPS Subunit Cgi121 Promotes Cell LongevityČlánek HOMER2, a Stereociliary Scaffolding Protein, Is Essential for Normal Hearing in Humans and MiceČlánek LRGUK-1 Is Required for Basal Body and Manchette Function during Spermatogenesis and Male FertilityČlánek The GATA Factor Regulates . Developmental Timing by Promoting Expression of the Family MicroRNAsČlánek Systems Biology of Tissue-Specific Response to Reveals Differentiated Apoptosis in the Tick VectorČlánek Phenotype Specific Analyses Reveal Distinct Regulatory Mechanism for Chronically Activated p53Článek The Nuclear Receptor DAF-12 Regulates Nutrient Metabolism and Reproductive Growth in NematodesČlánek The ATM Signaling Cascade Promotes Recombination-Dependent Pachytene Arrest in Mouse Spermatocytes
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2015 Číslo 3- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- NLRC5 Exclusively Transactivates MHC Class I and Related Genes through a Distinctive SXY Module
- Licensing of Primordial Germ Cells for Gametogenesis Depends on Genital Ridge Signaling
- A Genomic Duplication is Associated with Ectopic Eomesodermin Expression in the Embryonic Chicken Comb and Two Duplex-comb Phenotypes
- Genome-wide Association Study and Meta-Analysis Identify as Genome-wide Significant Susceptibility Gene for Bladder Exstrophy
- Mutations of Human , Encoding the Mitochondrial Asparaginyl-tRNA Synthetase, Cause Nonsyndromic Deafness and Leigh Syndrome
- Exome Sequencing in an Admixed Isolated Population Indicates Variants Confer a Risk for Specific Language Impairment
- Genome-Wide Association Studies in Dogs and Humans Identify as a Risk Variant for Cleft Lip and Palate
- Rapid Evolution of Recombinant for Xylose Fermentation through Formation of Extra-chromosomal Circular DNA
- The Ribosome Biogenesis Factor Nol11 Is Required for Optimal rDNA Transcription and Craniofacial Development in
- Methyl Farnesoate Plays a Dual Role in Regulating Metamorphosis
- Maternal Co-ordinate Gene Regulation and Axis Polarity in the Scuttle Fly
- Maternal Filaggrin Mutations Increase the Risk of Atopic Dermatitis in Children: An Effect Independent of Mutation Inheritance
- Inhibition of Telomere Recombination by Inactivation of KEOPS Subunit Cgi121 Promotes Cell Longevity
- Clonality and Evolutionary History of Rhabdomyosarcoma
- HOMER2, a Stereociliary Scaffolding Protein, Is Essential for Normal Hearing in Humans and Mice
- Methylation-Sensitive Expression of a DNA Demethylase Gene Serves As an Epigenetic Rheostat
- BREVIPEDICELLUS Interacts with the SWI2/SNF2 Chromatin Remodeling ATPase BRAHMA to Regulate and Expression in Control of Inflorescence Architecture
- Seizures Are Regulated by Ubiquitin-specific Peptidase 9 X-linked (USP9X), a De-Ubiquitinase
- The Fun30 Chromatin Remodeler Fft3 Controls Nuclear Organization and Chromatin Structure of Insulators and Subtelomeres in Fission Yeast
- A Cascade of Iron-Containing Proteins Governs the Genetic Iron Starvation Response to Promote Iron Uptake and Inhibit Iron Storage in Fission Yeast
- Mutation in MRPS34 Compromises Protein Synthesis and Causes Mitochondrial Dysfunction
- LRGUK-1 Is Required for Basal Body and Manchette Function during Spermatogenesis and Male Fertility
- Cis-Regulatory Mechanisms for Robust Olfactory Sensory Neuron Class-restricted Odorant Receptor Gene Expression in
- Effects on Murine Behavior and Lifespan of Selectively Decreasing Expression of Mutant Huntingtin Allele by Supt4h Knockdown
- HDAC4-Myogenin Axis As an Important Marker of HD-Related Skeletal Muscle Atrophy
- A Conserved Domain in the Scc3 Subunit of Cohesin Mediates the Interaction with Both Mcd1 and the Cohesin Loader Complex
- Selective and Genetic Constraints on Pneumococcal Serotype Switching
- Bacterial Infection Drives the Expression Dynamics of microRNAs and Their isomiRs
- The GATA Factor Regulates . Developmental Timing by Promoting Expression of the Family MicroRNAs
- Accumulation of Glucosylceramide in the Absence of the Beta-Glucosidase GBA2 Alters Cytoskeletal Dynamics
- Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities
- The Contribution of Alu Elements to Mutagenic DNA Double-Strand Break Repair
- Systems Biology of Tissue-Specific Response to Reveals Differentiated Apoptosis in the Tick Vector
- Tfap2a Promotes Specification and Maturation of Neurons in the Inner Ear through Modulation of Bmp, Fgf and Notch Signaling
- The Lysine Acetyltransferase Activator Brpf1 Governs Dentate Gyrus Development through Neural Stem Cells and Progenitors
- PHABULOSA Controls the Quiescent Center-Independent Root Meristem Activities in
- DNA Polymerase ζ-Dependent Lesion Bypass in Is Accompanied by Error-Prone Copying of Long Stretches of Adjacent DNA
- Examining the Evolution of the Regulatory Circuit Controlling Secondary Metabolism and Development in the Fungal Genus
- Zinc Finger Independent Genome-Wide Binding of Sp2 Potentiates Recruitment of Histone-Fold Protein Nf-y Distinguishing It from Sp1 and Sp3
- GAGA Factor Maintains Nucleosome-Free Regions and Has a Role in RNA Polymerase II Recruitment to Promoters
- Neurospora Importin α Is Required for Normal Heterochromatic Formation and DNA Methylation
- Ccr4-Not Regulates RNA Polymerase I Transcription and Couples Nutrient Signaling to the Control of Ribosomal RNA Biogenesis
- Phenotype Specific Analyses Reveal Distinct Regulatory Mechanism for Chronically Activated p53
- A Systems-Level Interrogation Identifies Regulators of Blood Cell Number and Survival
- Morphological Mutations: Lessons from the Cockscomb
- Genetic Interaction Mapping Reveals a Role for the SWI/SNF Nucleosome Remodeler in Spliceosome Activation in Fission Yeast
- The Role of China in the Global Spread of the Current Cholera Pandemic
- The Nuclear Receptor DAF-12 Regulates Nutrient Metabolism and Reproductive Growth in Nematodes
- A Zinc Finger Motif-Containing Protein Is Essential for Chloroplast RNA Editing
- Resistance to Gray Leaf Spot of Maize: Genetic Architecture and Mechanisms Elucidated through Nested Association Mapping and Near-Isogenic Line Analysis
- Small Regulatory RNA-Induced Growth Rate Heterogeneity of
- Mitochondrial Dysfunction Reveals the Role of mRNA Poly(A) Tail Regulation in Oculopharyngeal Muscular Dystrophy Pathogenesis
- Complex Genomic Rearrangements at the Locus Include Triplication and Quadruplication
- Male-Biased Aganglionic Megacolon in the TashT Mouse Line Due to Perturbation of Silencer Elements in a Large Gene Desert of Chromosome 10
- Sex Ratio Meiotic Drive as a Plausible Evolutionary Mechanism for Hybrid Male Sterility
- Tertiary siRNAs Mediate Paramutation in .
- RECG Maintains Plastid and Mitochondrial Genome Stability by Suppressing Extensive Recombination between Short Dispersed Repeats
- Escape from X Inactivation Varies in Mouse Tissues
- Opposite Phenotypes of Muscle Strength and Locomotor Function in Mouse Models of Partial Trisomy and Monosomy 21 for the Proximal Region
- Glycosyl Phosphatidylinositol Anchor Biosynthesis Is Essential for Maintaining Epithelial Integrity during Embryogenesis
- Hyperdiverse Gene Cluster in Snail Host Conveys Resistance to Human Schistosome Parasites
- The Class Homeodomain Factors and Cooperate in . Embryonic Progenitor Cells to Regulate Robust Development
- Recombination between Homologous Chromosomes Induced by Unrepaired UV-Generated DNA Damage Requires Mus81p and Is Suppressed by Mms2p
- Synergistic Interactions between Orthologues of Genes Spanned by Human CNVs Support Multiple-Hit Models of Autism
- Gene Networks Underlying Convergent and Pleiotropic Phenotypes in a Large and Systematically-Phenotyped Cohort with Heterogeneous Developmental Disorders
- The ATM Signaling Cascade Promotes Recombination-Dependent Pachytene Arrest in Mouse Spermatocytes
- Combinatorial Control of Light Induced Chromatin Remodeling and Gene Activation in
- Linking Aβ42-Induced Hyperexcitability to Neurodegeneration, Learning and Motor Deficits, and a Shorter Lifespan in an Alzheimer’s Model
- The Complex Contributions of Genetics and Nutrition to Immunity in
- NatB Domain-Containing CRA-1 Antagonizes Hydrolase ACER-1 Linking Acetyl-CoA Metabolism to the Initiation of Recombination during . Meiosis
- Transcriptomic Profiling of Reveals Reprogramming of the Crp Regulon by Temperature and Uncovers Crp as a Master Regulator of Small RNAs
- Osteopetrorickets due to Snx10 Deficiency in Mice Results from Both Failed Osteoclast Activity and Loss of Gastric Acid-Dependent Calcium Absorption
- A Genomic Portrait of Haplotype Diversity and Signatures of Selection in Indigenous Southern African Populations
- Sequence Features and Transcriptional Stalling within Centromere DNA Promote Establishment of CENP-A Chromatin
- Inhibits Neuromuscular Junction Growth by Downregulating the BMP Receptor Thickveins
- Replicative DNA Polymerase δ but Not ε Proofreads Errors in and in
- Unsaturation of Very-Long-Chain Ceramides Protects Plant from Hypoxia-Induced Damages by Modulating Ethylene Signaling in
- The Small Protein MntS and Exporter MntP Optimize the Intracellular Concentration of Manganese
- A Meta-analysis of Gene Expression Signatures of Blood Pressure and Hypertension
- Pervasive Variation of Transcription Factor Orthologs Contributes to Regulatory Network Evolution
- Network Analyses Reveal Novel Aspects of ALS Pathogenesis
- A Role for the Budding Yeast Separase, Esp1, in Ty1 Element Retrotransposition
- Nab3 Facilitates the Function of the TRAMP Complex in RNA Processing via Recruitment of Rrp6 Independent of Nrd1
- A RecA Protein Surface Required for Activation of DNA Polymerase V
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Clonality and Evolutionary History of Rhabdomyosarcoma
- Morphological Mutations: Lessons from the Cockscomb
- Maternal Filaggrin Mutations Increase the Risk of Atopic Dermatitis in Children: An Effect Independent of Mutation Inheritance
- Transcriptomic Profiling of Reveals Reprogramming of the Crp Regulon by Temperature and Uncovers Crp as a Master Regulator of Small RNAs
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy