期刊论文详细信息
EvoDevo
Evolution of transcription factor function as a mechanism for changing metazoan developmental gene regulatory networks
Veronica F Hinman1  Alys M Cheatle Jarvela1 
[1] Department of Biological Sciences, Carnegie Mellon University, 4400 5th Ave, Pittsburgh, PA 15213, USA
关键词: Novelty;    Development;    Gene regulatory network;    Transcription factor;   
Others  :  1121304
DOI  :  10.1186/2041-9139-6-3
 received in 2014-11-05, accepted in 2014-12-18,  发布年份 2015
PDF
【 摘 要 】

The form that an animal takes during development is directed by gene regulatory networks (GRNs). Developmental GRNs interpret maternally deposited molecules and externally supplied signals to direct cell-fate decisions, which ultimately leads to the arrangements of organs and tissues in the organism. Genetically encoded modifications to these networks have generated the wide range of metazoan diversity that exists today. Most studies of GRN evolution focus on changes to cis-regulatory DNA, and it was historically theorized that changes to the transcription factors that bind to these cis-regulatory modules (CRMs) contribute to this process only rarely. A growing body of evidence suggests that changes to the coding regions of transcription factors play a much larger role in the evolution of developmental gene regulatory networks than originally imagined. Just as cis-regulatory changes make use of modular binding site composition and tissue-specific modules to avoid pleiotropy, transcription factor coding regions also predominantly evolve in ways that limit the context of functional effects. Here, we review the recent works that have led to this unexpected change in the field of Evolution and Development (Evo-Devo) and consider the implications these studies have had on our understanding of the evolution of developmental processes.

【 授权许可】

   
2015 Cheatle Jarvela and Hinman; licensee BioMed Central.

【 预 览 】
附件列表
Files Size Format View
20150211030108362.pdf 303KB PDF download
Figure 1. 74KB Image download
【 图 表 】

Figure 1.

【 参考文献 】
  • [1]Davidson EH: The Regulatory Genome: Gene Regulatory Networks In Development And Evolution. Burlington, MA: Academic Press; 2010.
  • [2]Rubinstein M, de Souza FSJ: Evolution of transcriptional enhancers and animal diversity. Philos Trans R Soc Lond B Biol Sci. 2013, 368:20130017.
  • [3]Wittkopp PJ, Kalay G: Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet. 2012, 13:59-69.
  • [4]Wray GA: The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 2007, 8:206-16.
  • [5]Hinman VF, Nguyen A, Davidson EH: Caught in the evolutionary act: precise cis-regulatory basis of difference in the organization of gene networks of sea stars and sea urchins. Dev Biol. 2007, 312:584-95.
  • [6]Arnoult L, Su KFY, Manoel D, Minervino C, Magriña J, Gompel N, et al.: Emergence and Diversification of Fly Pigmentation Through Evolution of a Gene Regulatory Module. Science. 2013, 339:1423-6.
  • [7]Guerreiro I, Nunes A, Woltering JM, Casaca A, Nóvoa A, Vinagre T, et al.: Role of a polymorphism in a Hox/Pax-responsive enhancer in the evolution of the vertebrate spine. Proc Natl Acad Sci. 2013, 110:10682-6.
  • [8]Rogers WA, Salomone JR, Tacy DJ, Camino EM, Davis KA, Rebeiz M, et al.: Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity. PLoS Genet. 2013, 9:e1003740.
  • [9]Johnson DS, Mortazavi A, Myers RM, Wold B: Genome-wide mapping of in vivo protein-DNA interactions. Science. 2007, 316:1497-502.
  • [10]Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, et al.: Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science. 2010, 328:1036-40.
  • [11]Meader S, Ponting CP, Lunter G: Massive turnover of functional sequence in human and other mammalian genomes. Genome Res. 2010, 20:1335-43.
  • [12]McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ: A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell. 1984, 37:403-8.
  • [13]Duboule D, Dollé P: The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 1989, 8:1497-505.
  • [14]Ryan JF, Baxevanis AD: Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla. Biol Direct. 2007, 2:37. BioMed Central Full Text
  • [15]DuBuc TQ, Ryan JF, Shinzato C, Satoh N, Martindale MQ: Coral Comparative Genomics Reveal Expanded Hox Cluster in the Cnidarian–Bilaterian Ancestor. Integr Comp Biol. 2012, 52:835-41.
  • [16]Halder G, Callaerts P, Gehring WJ: Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science. 1995, 267:1788-92.
  • [17]McGinnis N, Kuziora MA, McGinnis W: Human Hox-4.2 and Drosophila deformed encode similar regulatory specificities in Drosophila embryos and larvae. Cell 1990, 63:969-76.
  • [18]Wang VY, Hassan BA, Bellen HJ, Zoghbi HY: Drosophila atonal fully rescues the phenotype of Math1 null mice: new functions evolve in new cellular contexts. Curr Biol CB. 2002, 12:1611-6.
  • [19]Carroll SB: Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom. New York, NY: Norton & Company: W. W; 2005.
  • [20]Carroll SB: Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell. 2008, 134:25-36.
  • [21]Britten RJ, Davidson EH: Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol. 1971, 46:111-38.
  • [22]Stern DL: Evolutionary developmental biology and the problem of variation. Evol Int J Org Evol. 2000, 54:1079-91.
  • [23]Lynch VJ, Wagner GP: Resurrecting the role of transcription factor change in developmental evolution. Evol Int J Org Evol. 2008, 62:2131-54.
  • [24]Hoekstra HE, Coyne JA: The locus of evolution: evo devo and the genetics of adaptation. Evol Int J Org Evol. 2007, 61:995-1016.
  • [25]Castanon I, Baylies MK: A Twist in fate: evolutionary comparison of Twist structure and function. Gene. 2002, 287:11-22.
  • [26]Kaestner KH, Knochel W, Martinez DE: Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 2000, 14:142-6.
  • [27]Laudet V, Hänni C, Stéhelin D, Duterque-Coquillaud M: Molecular phylogeny of the ETS gene family. Oncogene. 1999, 18:1351-9.
  • [28]Degnan BM, Vervoort M, Larroux C, Richards GS: Early evolution of metazoan transcription factors. Curr Opin Genet Dev. 2009, 19:591-9.
  • [29]Sebé-Pedrós A, de Mendoza A, Lang BF, Degnan BM, Ruiz-Trillo I: Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol. 2011, 28:1241-54.
  • [30]Holland PWH: Evolution of homeobox genes. Wiley Interdiscip Rev Dev Biol. 2013, 2:31-45.
  • [31]Pérez JC, Fordyce PM, Lohse MB, Hanson-Smith V, DeRisi JL, Johnson AD: How duplicated transcription regulators can diversify to govern the expression of nonoverlapping sets of genes. Genes Dev. 2014, 28:1272-7.
  • [32]Teichmann SA, Babu MM: Gene regulatory network growth by duplication. Nat Genet. 2004, 36:492-6.
  • [33]De Mendoza A, Sebé-Pedrós A, Šestak MS, Matejcic M, Torruella G, Domazet-Loso T, et al.: Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages. Proc Natl Acad Sci U S A. 2013, 110:E4858-66.
  • [34]Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, et al.: The Amphimedon queenslandica genome and the evolution of animal complexity. Nature. 2010, 466:720-6.
  • [35]Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999, 151:1531-45.
  • [36]Davidson CJ, Tirouvanziam R, Herzenberg LA, Lipsick JS: Functional evolution of the vertebrate Myb gene family B-Myb, but neither A-Myb nor c-Myb, complements Drosophila Myb in hemocytes. Genetics. 2005, 169:215-29.
  • [37]Davidson CJ, Guthrie EE, Lipsick JS: Duplication and maintenance of the Myb genes of vertebrate animals. Biol Open. 2013, 2:101-10.
  • [38]Ganter B, Lipsick JS: Myb and Oncogenesis. In Advances in Cancer Research, vol. 76. Edited by Vande Woude GF, Klein G. San Diego, CA: Academic Press; 1999:21-60.
  • [39]McKeown AN, Bridgham JT, Anderson DW, Murphy MN, Ortlund EA, Thornton JW: Evolution of DNA specificity in a transcription factor family produced a new gene regulatory module. Cell. 2014, 159:58-68.
  • [40]Eick GN, Colucci JK, Harms MJ, Ortlund EA, Thornton JW: Evolution of minimal specificity and promiscuity in steroid hormone receptors. PLoS Genet. 2012, 8:e1003072.
  • [41]Kostrouchova M, Kostrouch Z: Nuclear receptors in nematode development: natural experiments made by a phylum. Biochim Biophys Acta BBA - Gene Regul Mech 2014. doi: 10.1016/j.bbagrm.2014.06.016
  • [42]Robinson-Rechavi M, Maina CV, Gissendanner CR, Laudet V, Sluder A: Explosive lineage-specific expansion of the orphan nuclear receptor HNF4 in nematodes. J Mol Evol. 2005, 60:577-86.
  • [43]Sluder AE, Mathews SW, Hough D, Yin VP, Maina CV: The nuclear receptor superfamily has undergone extensive proliferation and diversification in nematodes. Genome Res. 1999, 9:103-20.
  • [44]Nowick K, Stubbs L: Lineage-specific transcription factors and the evolution of gene regulatory networks. Brief Funct Genomics. 2010, 9:65-78.
  • [45]Chung H-R, Löhr U, Jäckle H: Lineage-specific expansion of the zinc finger associated domain ZAD. Mol Biol Evol. 2007, 24:1934-43.
  • [46]Liu H, Chang L-H, Sun Y, Lu X, Stubbs L: Deep vertebrate roots for mammalian zinc finger transcription factor subfamilies. Genome Biol Evol. 2014, 6:510-25.
  • [47]Corsinotti A, Kapopoulou A, Gubelmann C, Imbeault M, Santoni de Sio FR, Rowe HM, et al.: Global and stage specific patterns of Krüppel-associated-box zinc finger protein gene expression in murine early embryonic cells. PLoS One. 2013, 8:e56721.
  • [48]Quenneville S, Turelli P, Bojkowska K, Raclot C, Offner S, Kapopoulou A, et al.: The KRAB-ZFP/KAP1 system contributes to the early embryonic establishment of site-specific DNA methylation patterns maintained during development. Cell Rep. 2012, 2:766-73.
  • [49]Bustamante CD, Fledel-Alon A, Williamson S, Nielsen R, Todd Hubisz M, Glanowski S, et al.: Natural selection on protein-coding genes in the human genome. Nature. 2005, 437:1153-7.
  • [50]Nowick K, Gernat T, Almaas E, Stubbs L: Differences in human and chimpanzee gene expression patterns define an evolving network of transcription factors in brain. Proc Natl Acad Sci. 2009, 106:22358-63.
  • [51]Koch BJ, Ryan JF, Baxevanis AD: The diversification of the LIM superclass at the base of the Metazoa increased subcellular complexity and promoted multicellular specialization. PLoS ONE. 2012, 7:e33261.
  • [52]Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM, et al.: Early evolution of the LIM homeobox gene family. BMC Biol. 2010, 8:4. BioMed Central Full Text
  • [53]Kawashima T, Kawashima S, Tanaka C, Murai M, Yoneda M, Putnam NH, et al.: Domain shuffling and the evolution of vertebrates. Genome Res. 2009, 19:1393-403.
  • [54]Nowick K, Fields C, Gernat T, Caetano-Anolles D, Kholina N, Stubbs L: Gain, loss and divergence in primate zinc-finger genes: a rich resource for evolution of gene regulatory differences between species. PLoS One. 2011, 6:e21553.
  • [55]Daburon V, Mella S, Plouhinec J-L, Mazan S, Crozatier M, Vincent A: The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates. BMC Evol Biol 2008, 8:131. BioMed Central Full Text
  • [56]Pocock R, Mione M, Hussain S, Maxwell S, Pontecorvi M, Aslam S, et al.: Neuronal function of Tbx20 conserved from nematodes to vertebrates. Dev Biol. 2008, 317:671-85.
  • [57]Gao Y, Lan Y, Ovitt CE, Jiang R: Functional equivalence of the zinc finger transcription factors Osr1 and Osr2 in mouse development. Dev Biol. 2009, 328:200-9.
  • [58]Hoser M, Potzner MR, Koch JMC, Bösl MR, Wegner M, Sock E: Sox12 deletion in the mouse reveals nonreciprocal redundancy with the related Sox4 and Sox11 transcription factors. Mol Cell Biol. 2008, 28:4675-87.
  • [59]Hanes SD, Brent R: DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell. 1989, 57:1275-83.
  • [60]Baker CR, Tuch BB, Johnson AD: Extensive DNA-binding specificity divergence of a conserved transcription regulator. Proc Natl Acad Sci U S A. 2011, 108:7493-8.
  • [61]Sayou C, Monniaux M, Nanao MH, Moyroud E, Brockington SF, Thévenon E, et al.: A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science. 2014, 343:645-8.
  • [62]Oliphant AR, Brandl CJ, Struhl K: Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Mol Cell Biol. 1989, 9:2944-9.
  • [63]Siggers T, Gordân R: Protein-DNA binding: complexities and multi-protein codes. Nucleic Acids Res. 2014, 42:2099-111.
  • [64]Berger MF, Bulyk ML: Protein binding microarrays (PBMs) for rapid, high-throughput characterization of the sequence specificities of DNA binding proteins. Methods Mol Biol Clifton NJ. 2006, 338:245-60.
  • [65]Berger MF, Philippakis AA, Qureshi AM, He FS, Estep PW, Bulyk ML: Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat Biotechnol. 2006, 24:1429-35.
  • [66]Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, Jaeger SA, et al.: Diversity and complexity in DNA recognition by transcription factors. Science. 2009, 324:1720-3.
  • [67]Gordân R, Murphy KF, McCord RP, Zhu C, Vedenko A, Bulyk ML: Curated collection of yeast transcription factor DNA binding specificity data reveals novel structural and gene regulatory insights. Genome Biol. 2011, 12:R125. BioMed Central Full Text
  • [68]Zhu C, Byers KJRP, McCord RP, Shi Z, Berger MF, Newburger DE, et al.: High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res. 2009, 19:556-66.
  • [69]Busser BW, Shokri L, Jaeger SA, Gisselbrecht SS, Singhania A, Berger MF, et al.: Molecular mechanism underlying the regulatory specificity of a Drosophila homeodomain protein that specifies myoblast identity. Dev Camb Engl. 2012, 139:1164-74.
  • [70]Wei G-H, Badis G, Berger MF, Kivioja T, Palin K, Enge M, et al.: Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J. 2010, 29:2147-60.
  • [71]Grove CA, De Masi F, Barrasa MI, Newburger DE, Alkema MJ, Bulyk ML, et al.: A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell. 2009, 138:314-27.
  • [72]Siggers T, Reddy J, Barron B, Bulyk ML: Diversification of transcription factor paralogs via noncanonical modularity in C2H2 zinc finger DNA binding. Mol Cell. 2014, 55:640-8.
  • [73]Nakagawa S, Gisselbrecht SS, Rogers JM, Hartl DL, Bulyk ML: DNA-binding specificity changes in the evolution of forkhead transcription factors. Proc Natl Acad Sci. 2013, 110:12349-54.
  • [74]Cheatle Jarvela AM, Brubaker L, Vedenko A, Gupta A, Armitage BA, Bulyk ML, et al.: Modular evolution of DNA binding preference of a Tbrain transcription factor provides a mechanism for modifying gene regulatory networks. Mol Biol Evol. 2014, 31:2672-88.
  • [75]Hedges SB, Dudley J, Kumar S: TimeTree: a public knowledge-base of divergence times among organisms. Bioinforma Oxf Engl. 2006, 22:2971-2.
  • [76]Hinman VF, Davidson EH: Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci U S A. 2007, 104:19404-9.
  • [77]McCauley BS, Weideman EP, Hinman VF: A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos. Dev Biol. 2010, 340:200-8.
  • [78]Croce J, Lhomond G, Lozano JC, Gache C: ske-T, a T-box gene expressed in the skeletogenic mesenchyme lineage of the sea urchin embryo. Mech Dev 2001, 107:159-62.
  • [79]Oliveri P, Carrick DM, Davidson EH: A regulatory gene network that directs micromere specification in the sea urchin embryo. Dev Biol. 2002, 246:209-28.
  • [80]Parker DS, White MA, Ramos AI, Cohen BA, Barolo S: The cis-regulatory logic of Hedgehog gradient responses: key roles for gli binding affinity, competition, and cooperativity. Sci Signal. 2011, 4:ra38.
  • [81]Ramos AI, Barolo S: Low-affinity transcription factor binding sites shape morphogen responses and enhancer evolution. Philos Trans R Soc B Biol Sci. 2013, 368:20130018.
  • [82]Rowan S, Siggers T, Lachke SA, Yue Y, Bulyk ML, Maas RL: Precise temporal control of the eye regulatory gene Pax6 via enhancer-binding site affinity. Genes Dev. 2010, 24:980-5.
  • [83]Keyte AL, Smith KK: Heterochrony and developmental timing mechanisms: Changing ontogenies in evolution. Semin Cell Dev Biol. 2014, 34C:99-107.
  • [84]Smith KK: Time’s arrow: heterochrony and the evolution of development. Int J Dev Biol. 2003, 47:613-21.
  • [85]Taneri B, Snyder B, Novoradovsky A, Gaasterland T: Alternative splicing of mouse transcription factors affects their DNA-binding domain architecture and is tissue specific. Genome Biol. 2004, 5:R75. BioMed Central Full Text
  • [86]Blekhman R, Marioni JC, Zumbo P, Stephens M, Gilad Y: Sex-specific and lineage-specific alternative splicing in primates. Genome Res. 2010, 20:180-9.
  • [87]Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, Carroll SB: The regulation and evolution of a genetic switch controlling sexually dimorphic traits in drosophila. Cell. 2008, 134:610-23.
  • [88]Burtis KC, Baker BS: Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell. 1989, 56:997-1010.
  • [89]Garrett-Engele CM, Siegal ML, Manoli DS, Williams BC, Li H, Baker BS: intersex, a gene required for female sexual development in Drosophila, is expressed in both sexes and functions together with doublesex to regulate terminal differentiation. Dev Camb Engl 2002, 129:4661-75.
  • [90]Löhr U, Pick L: Cofactor-interaction motifs and the cooption of a homeotic Hox protein into the segmentation pathway of Drosophila melanogaster. Curr Biol CB. 2005, 15:643-9.
  • [91]Heffer A, Shultz JW, Pick L: Surprising flexibility in a conserved Hox transcription factor over 550 million years of evolution. Proc Natl Acad Sci U S A. 2010, 107:18040-5.
  • [92]Smith ST, Jaynes JB: A conserved region of engrailed, shared among all en-, gsc-, Nk1-, Nk2- and msh-class homeoproteins, mediates active transcriptional repression in vivo. Dev Camb Engl. 1996, 122:3141-50.
  • [93]Tolkunova EN, Fujioka M, Kobayashi M, Deka D, Jaynes JB: Two distinct types of repression domain in engrailed: one interacts with the groucho corepressor and is preferentially active on integrated target genes. Mol Cell Biol. 1998, 18:2804-14.
  • [94]Hittinger CT, Carroll SB: Evolution of an insect-specific GROUCHO-interaction motif in the ENGRAILED selector protein. Evol Dev. 2008, 10:537-45.
  • [95]Brayer KJ, Lynch VJ, Wagner GP: Evolution of a derived protein-protein interaction between HoxA11 and Foxo1a in mammals caused by changes in intramolecular regulation. Proc Natl Acad Sci U S A. 2011, 108:E414-20.
  • [96]Lynch VJ, Tanzer A, Wang Y, Leung FC, Gellersen B, Emera D, et al.: Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc Natl Acad Sci U S A. 2008, 105:14928-33.
  • [97]Lynch VJ, Brayer K, Gellersen B, Wagner GP: HoxA-11 and FOXO1A cooperate to regulate decidual prolactin expression: towards inferring the core transcriptional regulators of decidual genes. PLoS One. 2009, 4:e6845.
  • [98]Van Loosdregt J, Coffer PJ: Post-translational modification networks regulating FOXP3 function. Trends Immunol. 2014, 35:368-78.
  • [99]Prasad MS, Sauka-Spengler T, LaBonne C: Induction of the neural crest state: Control of stem cell attributes by gene regulatory, post-transcriptional and epigenetic interactions. Dev Biol. 2012, 366:10-21.
  • [100]Kim DS, Hahn Y: Gains of ubiquitylation sites in highly conserved proteins in the human lineage. BMC Bioinformatics. 2012, 13:306. BioMed Central Full Text
  • [101]Kim DS, Hahn Y: Identification of novel phosphorylation modification sites in human proteins that originated after the human-chimpanzee divergence. Bioinforma Oxf Engl. 2011, 27:2494-501.
  • [102]Enard W, Przeworski M, Fisher SE, Lai CSL, Wiebe V, Kitano T, et al.: Molecular evolution of FOXP2, a gene involved in speech and language. Nature. 2002, 418:869-72.
  • [103]Tsui D, Vessey JP, Tomita H, Kaplan DR, Miller FD: FoxP2 regulates neurogenesis during embryonic cortical development. J Neurosci Off J Soc Neurosci. 2013, 33:244-58.
  • [104]Ronshaugen M, McGinnis N, McGinnis W: Hox protein mutation and macroevolution of the insect body plan. Nature. 2002, 415:914-7.
  • [105]Taghli-Lamallem O, Hsia C, Ronshaugen M, McGinnis W: Context-dependent regulation of Hox protein functions by CK2 phosphorylation sites. Dev Genes Evol. 2008, 218:321-32.
  • [106]Bourbon HM, Martin-Blanco E, Rosen D, Kornberg TB: Phosphorylation of the Drosophila engrailed protein at a site outside its homeodomain enhances DNA binding. J Biol Chem. 1995, 270:11130-9.
  • [107]Jaffe L, Ryoo HD, Mann RS: A role for phosphorylation by casein kinase II in modulating Antennapedia activity in Drosophila. Genes Dev. 1997, 11:1327-40.
  • [108]Lynch VJ, May G, Wagner GP: Regulatory evolution through divergence of a phosphoswitch in the transcription factor CEBPB. Nature. 2011, 480:383-6.
  • [109]Maricic T, Günther V, Georgiev O, Gehre S, Curlin M, Schreiweis C, et al.: A recent evolutionary change affects a regulatory element in the human FOXP2 gene. Mol Biol Evol. 2013, 30:844-52.
  • [110]Coolon JD, McManus CJ, Stevenson KR, Graveley BR, Wittkopp PJ: Tempo and mode of regulatory evolution in Drosophila. Genome Res. 2014, 24:797-808.
  文献评价指标  
  下载次数:0次 浏览次数:12次