Gene regulatory evolution and the origin of macroevolutionary novelties: Insights from the neural crest

Genesis

Volumn 51, Issue 7, 2013, Pages 457-470

  Van Otterloo, Eric ^a   Cornell, Robert A ^a   Medeiros, Daniel Meulemans ^b   Garnett, Aaron T ^b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Development; Evolution; Neural crest; Transcription

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7; TRANSCRIPTION FACTOR SOX; TRANSCRIPTION FACTOR SOX10;

CELL DIFFERENTIATION; CELL DIVISION; CELL MOTION; CELL TYPE; GENE; GENE DOSAGE; GENE DUPLICATION; GENE REGULATORY NETWORK; GENOME; HUMAN; MUTATION; NEURAL CREST; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY SEQUENCE; REVIEW;

DEVELOPMENT; EVOLUTION; NEURAL CREST; TRANSCRIPTION;

ANIMALS; BIOLOGICAL EVOLUTION; CHORDATA; EVOLUTION, MOLECULAR; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; NEURAL CREST; NEURAL PLATE; PHYLOGENY;

CHORDATA; INVERTEBRATA; VERTEBRATA;

EID: 84880703760     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22403     Document Type: Review

References (97)

1. Abitua PB, Wagner E, Navarrete IA, Levine M. 2012. Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature 492:104-107.
2. Bajolle F, Zaffran S, Kelly RG, Hadchouel J, Bonnet D, Brown NA, Buckingham ME. 2006. Rotation of the myocardial wall of the outflow tract is implicated in the normal positioning of the great arteries. Circ Res 98:421-428.
3. Basch ML, Bronner-Fraser M, Garcia-Castro MI. 2006. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441:218-222.
4. Bell KM, Western PS, Sinclair AH. 2000. SOX8 expression during chick embryogenesis. Mech Dev 94:257-260.
5. Bowles J, Schepers G, Koopman P. 2000. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227:239-255.
6. Brewer S, Feng W, Huang J, Sullivan S, Williams T. 2004. Wnt1-Cre-mediated deletion of AP-2alpha causes multiple neural crest-related defects. Dev Biol 267:135-152.
7. Brewer S, Jiang X, Donaldson S, Williams T, Sucov HM. 2002. Requirement for AP-2alpha in cardiac outflow tract morphogenesis. Mech Dev 110:139-149.
8. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, Nave KA, Birchmeier C, Wegner M. 2001. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15:66-78.
9. Brunet FG, Roest Crollius H, Paris M, Aury JM, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M. 2006. Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23:1808-1816.
10. Buckingham M, Relaix F. 2007. The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu Rev Cell Dev Biol 23:645-673.
11. Cande J, Goltsev Y, Levine MS. 2009. Conservation of enhancer location in divergent insects. Proc Natl Acad Sci USA 106:14414-14419.
12. Carney TJ, Dutton KA, Greenhill E, Delfino-Machin M, Dufourcq P, Blader P, Kelsh RN. 2006. A direct role for Sox10 in specification of neural crest-derived sensory neurons. Development 133:4619-4630.
13. Cheung M, Briscoe J. 2003. Neural crest development is regulated by the transcription factor Sox9. Development 130:5681-5693.
14. Cheung M, Chaboissier MC, Mynett A, Hirst E, Schedl A, Briscoe J. 2005. The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 8:179-192.
15. Conant GC, Wagner A. 2003. Asymmetric sequence divergence of duplicate genes. Genome Res 13:2052-2058.
16. Cossais F, Sock E, Hornig J, Schreiner S, Kellerer S, Bosl MR, Russell S, Wegner M. 2010. Replacement of mouse Sox10 by the Drosophila ortholog Sox100B provides evidence for co-option of SoxE proteins into vertebrate-specific gene-regulatory networks through altered expression. Dev Biol 341:267-281.
17. Crocker J, Tamori Y, Erives A. 2008. Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 6:e263.
18. Davidson EH, McClay DR, Hood L. 2003. Regulatory gene networks and the properties of the developmental process. Proc Natl Acad Sci USA 100:1475-1480.
19. de Croze N, Maczkowiak F, Monsoro-Burq AH. 2011. Reiterative AP2a activity controls sequential steps in the neural crest gene regulatory network. Proc Natl Acad Sci USA 108:155-160.
20. Depew MJ, Lufkin T, Rubenstein JL. 2002. Specification of jaw subdivisions by Dlx genes. Science 298:381-385.
21. Dirksen ML, Jamrich M. 1995. Differential expression of fork head genes during early Xenopus and zebrafish development. Dev Genet 17:107-116.
22. Dottori M, Gross MK, Labosky P, Goulding M. 2001. The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 128:4127-4138.
23. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, Rauch J, Geisler R, Haffter P, Kelsh RN. 2001. Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128:4113-4125.
24. Eichenlaub MP, Ettwiller L. 2011. De novo genesis of enhancers in vertebrates. PLoS Biol 9:e1001188.
25. Elworthy S, Lister JA, Carney TJ, Raible DW, Kelsh RN. 2003. Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130:2809-2818.
26. Fisher S, Grice EA, Vinton RM, Bessling SL, McCallion AS. 2006. Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 312:276-279.
27. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545.
28. Franz T. 1993. The Splotch (Sp1H) and Splotch-delayed (Spd) alleles: Differential phenotypic effects on neural crest and limb musculature. Anat Embryol (Berl) 187:371-377.
29. Franz T, Kothary R. 1993. Characterization of the neural crest defect in Splotch (Sp1H) mutant mice using a lacZ transgene. Brain Res Dev Brain Res 72:99-105.
30. Franz T, Kothary R, Surani MA, Halata Z, Grim M. 1993. The Splotch mutation interferes with muscle development in the limbs. Anat Embryol (Berl) 187:153-160.
31. Gilmour DT, Maischein HM, Nusslein-Volhard C. 2002. Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 34:577-588.
32. Green SA, Bronner ME. 2013. Gene duplications and the early evolution of neural crest development. Semin Cell Dev Biol 24:95-100.
33. Hadrys T, DeSalle R, Sagasser S, Fischer N, Schierwater B. 2005. The Trichoplax PaxB gene: A putative Proto-PaxA/B/C gene predating the origin of nerve and sensory cells. Mol Biol Evol 22:1569-1578.
34. Hall BK, Gillis JA. 2013. Incremental evolution of the neural crest, neural crest cells and neural crest-derived skeletal tissues. J Anat 222:19-31.
35. Hare EE, Peterson BK, Iyer VN, Meier R, Eisen MB. 2008. Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet 4:e1000106.
36. Hayashi S, Rocancourt D, Buckingham M, Relaix F. 2011. Lack of in vivo functional compensation between Pax family groups II and III in rodents. Mol Biol Evol 28:2787-2798.
37. Hittinger CT, Carroll SB. 2007. Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449:677-681.
38. Hoffman TL, Javier AL, Campeau SA, Knight RD, Schilling TF. 2007. Tfap2 transcription factors in zebrafish neural crest development and ectodermal evolution. J Exp Zool B Mol Dev Evol 308:679-691.
39. Holland LZ. 2013. Evolution of new characters after whole genome duplications: Insights from amphioxus. Semin Cell Dev Biol 24:101-109.
40. Holland ND, Holland LZ, Kozmik Z. 1995. An amphioxus Pax gene, AmphiPax-1, expressed in embryonic endoderm, but not in mesoderm: Implications for the evolution of class I paired box genes. Mol Mar Biol Biotechnol 4:206-214.
41. Holland PW. 1999. The effect of gene duplication on homology. Novartis Found Symp 222:226-236; discussion 236-242.
42. Hong CS, Saint-Jeannet JP. 2005. Sox proteins and neural crest development. Semin Cell Dev Biol 16:694-703.
43. Hughes AL. 1994. The evolution of functionally novel proteins after gene duplication. Proc Biol Sci 256:119-124.
44. Imai KS, Satoh N, Satou Y. 2002. An essential role of a FoxD gene in notochord induction in Ciona embryos. Development 129:3441-3453.
45. Jeffery WR. 2006. Ascidian neural crest-like cells: Phylogenetic distribution, relationship to larval complexity, and pigment cell fate. J Exp Zool B Mol Dev Evol 306:470-480.
46. Jeffery WR. 2007. Chordate ancestry of the neural crest: New insights from ascidians. Semin Cell Dev Biol 18:481-491.
47. Jeffery WR, Strickler AG, Yamamoto Y. 2004. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431:696-699.
48. Kalay G, Wittkopp PJ. 2010. Nomadic enhancers: Tissue-specific cis-regulatory elements of yellow have divergent genomic positions among Drosophila species. PLoS Genet 6:e1001222.
49. Kapur RP. 1999. Early death of neural crest cells is responsible for total enteric aganglionosis in Sox10(Dom)/Sox10(Dom) mouse embryos. Pediatr Dev Pathol 2:559-569.
50. Kellerer S, Schreiner S, Stolt CC, Scholz S, Bosl MR, Wegner M. 2006. Replacement of the Sox10 transcription factor by Sox8 reveals incomplete functional equivalence. Development 133:2875-2886.
51. Kim J, Lo L, Dormand E, Anderson DJ. 2003. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38:17-31.
52. Knight RD, Nair S, Nelson SS, Afshar A, Javidan Y, Geisler R, Rauch GJ, Schilling TF. 2003. lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development 130:5755-5768.
53. Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV. 2002. Selection in the evolution of gene duplications. Genome Biol 3:RESEARCH0008.
54. Kundaje A, Kyriazopoulou-Panagiotopoulou S, Libbrecht M, Smith CL, Raha D, Winters EE, Johnson SM, Snyder M, Batzoglou S, Sidow A. 2012. Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements. Genome Res 22:1735-1747.
55. Lacosta AM, Muniesa P, Ruberte J, Sarasa M, Dominguez L. 2005. Novel expression patterns of Pax3/Pax7 in early trunk neural crest and its melanocyte and non-melanocyte lineages in amniote embryos. Pigment Cell Res 18:243-251.
56. Lakiza O, Miller S, Bunce A, Lee EM, McCauley DW. 2011. SoxE gene duplication and development of the lamprey branchial skeleton: Insights into development and evolution of the neural crest. Dev Biol 359:149-161.
57. Lang D, Epstein JA. 2003. Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum Mol Genet 12:937-945.
58. Li W, Cornell RA. 2007. Redundant activities of Tfap2a and Tfap2c are required for neural crest induction and development of other non-neural ectoderm derivatives in zebrafish embryos. Dev Biol 304:338-354.
59. Luo T, Lee YH, Saint-Jeannet JP, Sargent TD. 2003. Induction of neural crest in Xenopus by transcription factor AP2alpha. Proc Natl Acad Sci USA 100:532-537.
60. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151-1155.
61. Maczkowiak F, Mateos S, Wang E, Roche D, Harland R, Monsoro-Burq AH. 2010. The Pax3 and Pax7 paralogs cooperate in neural and neural crest patterning using distinct molecular mechanisms, in Xenopus laevis embryos. Dev Biol 340:381-396.
62. Maka M, Stolt CC, Wegner M. 2005. Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Dev Biol 277:155-169.
63. Mansouri A, Stoykova A, Torres M, Gruss P. 1996. Dysgenesis of cephalic neural crest derivatives in Pax7-/- mutant mice. Development 122:831-838.
64. McCauley DW, Bronner-Fraser M. 2006. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441:750-752.
65. Merzdorf CS. 2007. Emerging roles for zic genes in early development. Dev Dyn 236:922-940.
66. Meulemans D, Bronner-Fraser M. 2002. Amphioxus and lamprey AP-2 genes: Implications for neural crest evolution and migration patterns. Development 129:4953-4962.
67. Meulemans D, Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7:291-299.
68. Meulemans D, Bronner-Fraser M. 2005. Central role of gene cooption in neural crest evolution. J Exp Zool B Mol Dev Evol 304:298-303.
69. Meulemans D, Bronner-Fraser M. 2007. Insights from amphioxus into the evolution of vertebrate cartilage. PLoS One 2:e787.
70. Meulemans D, McCauley D, Bronner-Fraser M. 2003. Id expression in amphioxus and lamprey highlights the role of gene cooption during neural crest evolution. Dev Biol 264:430-442.
71. Micale L, Loviglio MN, Manzoni M, Fusco C, Augello B, Migliavacca E, Cotugno G, Monti E, Borsani G, Reymond A, Merla G. 2012. A fish-specific transposable element shapes the repertoire of p53 target genes in zebrafish. PLoS One 7:e46642.
72. Minchin JE, Hughes SM. 2008. Sequential actions of Pax3 and Pax7 drive xanthophore development in zebrafish neural crest. Dev Biol 317:508-522.
73. Minguillon C, Gibson-Brown JJ, Logan MP. 2009. Tbx4/5 gene duplication and the origin of vertebrate paired appendages. Proc Natl Acad Sci USA 106:21726-21730.
74. Monsoro-Burq AH, Wang E, Harland R. 2005. Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev Cell 8:167-178.
75. Murdoch B, DelConte C, Garcia-Castro MI. 2012. Pax7 lineage contributions to the mammalian neural crest. PLoS One 7:e41089.
76. O'Brien EK, d'Alencon C, Bonde G, Li W, Schoenebeck J, Allende ML, Gelb BD, Yelon D, Eisen JS, Cornell RA. 2004. Transcription factor Ap-2alpha is necessary for development of embryonic melanophores, autonomic neurons and pharyngeal skeleton in zebrafish. Dev Biol 265:246-261.
77. Ohno S. 1970. Evolution by gene duplication. Berlin, New York: Springer-Verlag.
78. Piatigorsky J. 1990. Molecular biology: Recent studies on enzyme/crystallins and alpha-crystallin gene expression. Exp Eye Res 50:725-728.
79. Pohl BS, Knochel W. 2002. Temporal and spatial expression patterns of FoxD2 during the early development of Xenopus laevis. Mech Dev 111:181-184.
80. Rebeiz M, Jikomes N, Kassner VA, Carroll SB. 2011. Evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences. Proc Natl Acad Sci USA 108:10036-10043.
81. Reiprich S, Stolt CC, Schreiner S, Parlato R, Wegner M. 2008. SoxE proteins are differentially required in mouse adrenal gland development. Mol Biol Cell 19:1575-1586.
82. Relaix F, Rocancourt D, Mansouri A, Buckingham M. 2004. Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev 18:1088-1105.
83. Roth S, Stein D, Nusslein-Volhard C. 1989. A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59:1189-1202.
84. Sato T, Sasai N, Sasai Y. 2005. Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132:2355-2363.
85. Southard-Smith EM, Kos L, Pavan WJ. 1998. Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nat Genet 18:60-64.
86. Stock DW, Ellies DL, Zhao Z, Ekker M, Ruddle FH, Weiss KM. 1996. The evolution of the vertebrate Dlx gene family. Proc Natl Acad Sci USA 93:10858-10863.
87. Stolt CC, Lommes P, Friedrich RP, Wegner M. 2004. Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy. Development 131:2349-2358.
88. Tremblay P, Kessel M, Gruss P. 1995. A transgenic neuroanatomical marker identifies cranial neural crest deficiencies associated with the Pax3 mutant Splotch. Dev Biol 171:317-329.
89. Van Otterloo E, Li W, Garnett A, Cattell M, Medeiros DM, Cornell RA. 2012. Novel Tfap2-mediated control of soxE expression facilitated the evolutionary emergence of the neural crest. Development 139:720-730.
90. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, Pierce BG, Dong X, Kundaje A, Cheng Y, Rando OJ, Birney E, Myers RM, Noble WS, Snyder M, Weng Z. 2012. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res 22:1798-1812.
91. Wang Q, Fang WH, Krupinski J, Kumar S, Slevin M, Kumar P. 2008. Pax genes in embryogenesis and oncogenesis. J Cell Mol Med 12:2281-2294.
92. Wang T, Zeng J, Lowe CB, Sellers RG, Salama SR, Yang M, Burgess SM, Brachmann RK, Haussler D. 2007. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci USA 104:18613-18618.
93. Watanabe Y, Duprez D, Monsoro-Burq AH, Vincent C, Le Douarin NM. 1998. Two domains in vertebral development: Antagonistic regulation by SHH and BMP4 proteins. Development 125:2631-2639.
94. Yu JK, Holland ND, Holland LZ. 2002. An amphioxus winged helix/forkhead gene, AmphiFoxD: Insights into vertebrate neural crest evolution. Dev Dyn 225:289-297.
95. Yu JK, Mazet F, Chen YT, Huang SW, Jung KC, Shimeld SM. 2008a. The Fox genes of Branchiostoma floridae. Dev Genes Evol 218:629-638.
96. Yu JK, Meulemans D, McKeown SJ, Bronner-Fraser M. 2008b. Insights from the amphioxus genome on the origin of vertebrate neural crest. Genome Res 18:1127-1132.
97. Zhang P, Gu Z, Li WH. 2003. Different evolutionary patterns between young duplicate genes in the human genome. Genome Biol 4:R56.