Evolution of vertebrate central nervous system is accompanied by novel expression changes of duplicate genes

Journal of Genetics and Genomics

Volumn 38, Issue 12, 2011, Pages 577-584

  Chen, Yuan ^a,b   Ding, Yun ^a,b   Zhang, Zuming ^a,b   Wang, Wen ^a   Chen, Jun Yuan ^c   Ueno, Naoto ^d   Mao, Bingyu ^a  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NANJING UNIVERSITY   (China)

^d NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

Amphioxus; Central nervous system evolution; Expression pattern; Gene duplication; Xenopus

Indexed keywords

ARTICLE; BRACHIOSTOMA BELCHERI; BRANCHIOSTOMA; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DUPLICATE GENE; EMBRYO; EMBRYO DEVELOPMENT; GENE DUPLICATION; GENE EXPRESSION; IN SITU HYBRIDIZATION; NONHUMAN; RHOMBENCEPHALON; TELENCEPHALON; VERTEBRATE; XENOPUS LAEVIS;

AMPHIBIANS; ANIMALS; CENTRAL NERVOUS SYSTEM; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENES, DUPLICATE; HUMANS; PHYLOGENY; VERTEBRATES; XENOPUS;

BRANCHIOSTOMA LANCEOLATUM; INVERTEBRATA; VERTEBRATA; XENOPUS LAEVIS;

EID: 84855198881     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2011.10.004     Document Type: Article

References (54)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Baez M.V., Boccaccio G.L. Mammalian Smaug is a translational repressor that forms cytoplasmic foci similar to stress granules. J. Biol. Chem. 2005, 280:43131-43140.
3. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36.
4. Carroll S.B., Grenier J.K., Weatherbee S.D. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design 2004, Blackwell Publishing, Malden, MA. second ed.
5. Castro L.F., Rasmussen S.L., Holland P.W., Holland N.D., Holland L.Z. A Gbx homeobox gene in amphioxus: insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary. Dev. Biol. 2006, 295:40-51.
6. Catchen J.M., Conery J.S., Postlethwait J.H. Automated identification of conserved synteny after whole-genome duplication. Genome Res. 2009, 19:1497-1505.
7. Chen J.Y. Early crest animals and the insight they provide into the evolutionary origin of craniates. Genesis 2008, 46:623-639.
8. Davidson E.H., Erwin D.H. Gene regulatory networks and the evolution of animal body plans. Science 2006, 311:796-800.
9. de Martino S., Yan Y.L., Jowett T., Postlethwait J.H., Varga Z.M., Ashworth A., Austin C.A. Expression of sox11 gene duplicates in zebrafish suggests the reciprocal loss of ancestral gene expression patterns in development. Dev. Dyn. 2000, 217:279-292.
10. Dehal P., Boore J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 2005, 3:e314.
11. Delsuc F., Brinkmann H., Chourrout D., Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006, 439:965-968.
12. Donoghue P.C., Purnell M.A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 2005, 20:312-319.
13. Gawantka V., Delius H., Hirschfeld K., Blumenstock C., Niehrs C. Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1. EMBO J. 1995, 14:6268-6279.
14. Glardon S., Holland L.Z., Gehring W.J., Holland N.D. Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): insights into eye and photoreceptor evolution. Development 1998, 125:2701-2710.
15. Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 1998, 391:357-362.
16. Harris C.D., Ermak G., Davies K.J. Multiple roles of the DSCR1 (Adapt78 or RCAN1) gene and its protein product calcipressin 1 (or RCAN1) in disease. Cell Mol. Life Sci. 2005, 62:2477-2486.
17. Holland L.Z., Holland N.D. Chordate origins of the vertebrate central nervous system. Curr. Opin. Neurobiol. 1999, 9:596-602.
18. Holland L.Z., Short S. Gene duplication, co-option and recruitment during the origin of the vertebrate brain from the invertebrate chordate brain. Brain Behav. Evol. 2008, 72:91-105.
19. Holland L.Z., Laudet V., Schubert M. The chordate amphioxus: an emerging model organism for developmental biology. Cell Mol. Life Sci. 2004, 61:2290-2308.
20. Holland L.Z., Albalat R., Azumi K., Benito-Gutierrez E., Blow M.J., Bronner-Fraser M., Brunet F., Butts T., Candiani S., Dishaw L.J., Ferrier D.E., Garcia-Fernandez J., Gibson-Brown J.J., Gissi C., Godzik A., Hallbook F., Hirose D., Hosomichi K., Ikuta T., Inoko H., Kasahara M., Kasamatsu J., Kawashima T., Kimura A., Kobayashi M., Kozmik Z., Kubokawa K., Laudet V., Litman G.W., McHardy A.C., Meulemans D., Nonaka M., Olinski R.P., Pancer Z., Pennacchio L.A., Pestarino M., Rast J.P., Rigoutsos I., Robinson-Rechavi M., Roch G., Saiga H., Sasakura Y., Satake M., Satou Y., Schubert M., Sherwood N., Shiina T., Takatori N., Tello J., Vopalensky P., Wada S., Xu A., Ye Y., Yoshida K., Yoshizaki F., Yu J.K., Zhang Q., Zmasek C.M., de Jong P.J., Osoegawa K., Putnam N.H., Rokhsar D.S., Satoh N., Holland P.W. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 2008, 18:1100-1111.
21. Holland N.D., Chen J. Origin and early evolution of the vertebrates: new insights from advances in molecular biology, anatomy, and palaeontology. Bioessays 2001, 23:142-151.
22. Holland P.W. Wholemount in situ hybridization to amphioxus embryos. Methods Mol. Biol. 1999, 97:641-644.
23. Holland P.W., Garcia-Fernandez J., Williams N.A., Sidow A. Gene duplications and the origins of vertebrate development. Dev. Suppl. 1994 1994, 125-133.
24. Hughes A.L. The evolution of functionally novel proteins after gene duplication. Proc. Biol. Sci. 1994, 256:119-124.
25. Imai K.S., Satoh N., Satou Y. Region specific gene expressions in the central nervous system of the ascidian embryo. Gene Expr. Patterns 2002, 2:319-321.
26. Jeffery W.R. Ascidian neural crest-like cells: phylogenetic distribution, relationship to larval complexity, and pigment cell fate. J. Exp. Zool. B Mol. Dev. Evol. 2006, 306:470-480.
27. Jeffery W.R., Strickler A.G., Yamamoto Y. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 2004, 431:696-699.
28. Jeffery W.R., Chiba T., Krajka F.R., Deyts C., Satoh N., Joly J.S. Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: insights into the ancestry and evolution of the neural crest. Dev. Biol. 2008, 324:152-160.
29. Kasahara M. The 2R hypothesis: an update. Curr. Opin. Immunol. 2007, 19:547-552.
30. Kohler M., Hirschberg B., Bond C.T., Kinzie J.M., Marrion N.V., Maylie J., Adelman J.P. Small-conductance, calcium-activated potassium channels from mammalian brain. Science 1996, 273:1709-1714.
31. Kuraku S., Meyer A. The evolution and maintenance of Hox gene clusters in vertebrates and the teleost-specific genome duplication. Int. J. Dev. Biol. 2009, 53:765-773.
32. Liao B.Y., Zhang J. Low rates of expression profile divergence in highly expressed genes and tissue-specific genes during mammalian evolution. Mol. Biol. Evol. 2006, 23:1119-1128.
33. Lynch M., Conery J.S. The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155.
34. Meulemans D., Bronner-Fraser M. Insights from amphioxus into the evolution of vertebrate cartilage. PLoS ONE 2007, 2:e787.
35. Meyer A., Schartl M. Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell Biol. 1999, 11:699-704.
36. Morel N. Neurotransmitter release: the dark side of the vacuolar-H+ATPase. Biol. Cell 2003, 95:453-457.
37. Ohno S. Evolution by Gene Duplication 1970, Springer-Verlag, Berlin, Germany.
38. Pietri T., Easley-Neal C., Wilson C., Washbourne P. Six cadm/SynCAM genes are expressed in the nervous system of developing zebrafish. Dev. Dyn. 2008, 237:233-246.
39. Putnam N.H., Butts T., Ferrier D.E., Furlong R.F., Hellsten U., Kawashima T., Robinson-Rechavi M., Shoguchi E., Terry A., Yu J.K., Benito-Gutierrez E.L., Dubchak I., Garcia-Fernandez J., Gibson-Brown J.J., Grigoriev I.V., Horton A.C., de Jong P.J., Jurka J., Kapitonov V.V., Kohara Y., Kuroki Y., Lindquist E., Lucas S., Osoegawa K., Pennacchio L.A., Salamov A.A., Satou Y., Sauka-Spengler T., Schmutz J., Shin I.T., Toyoda A., Bronner-Fraser M., Fujiyama A., Holland L.Z., Holland P.W., Satoh N., Rokhsar D.S. The amphioxus genome and the evolution of the chordate karyotype. Nature 2008, 453:1064-1071.
40. Rosahl T.W., Spillane D., Missler M., Herz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., Sudhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 1995, 375:488-493.
41. Schubert M., Escriva H., Xavier-Neto J., Laudet V. Amphioxus and tunicates as evolutionary model systems. Trends Ecol. Evol. 2006, 21:269-277.
42. Semon M., Wolfe K.H. Consequences of genome duplication. Curr. Opin. Genet. Dev. 2007, 17:505-512.
43. Stansberg C., Vik-Mo A.O., Holdhus R., Breilid H., Srebro B., Petersen K., Jorgensen H.A., Jonassen I., Steen V.M. Gene expression profiles in rat brain disclose CNS signature genes and regional patterns of functional specialisation. BMC Genomics 2007, 8:94.
44. Su A., Wiltshire T., Batalov S., Lapp H., Ching K., Block D., Zhang J., Soden R., Hayakawa M., Kreiman G. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA 2004, 101:6062.
45. Takahashi T. The evolutionary origins of vertebrate midbrain and MHB: insights from mouse, amphioxus and ascidian Dmbx homeobox genes. Brain Res. Bull. 2005, 66:510-517.
46. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
47. Tatusov R.L., Koonin E.V., Lipman D.J. A genomic perspective on protein families. Science 1997, 278:631-637.
48. Teichmann S.A., Babu M.M. Gene regulatory network growth by duplication. Nat. Genet. 2004, 36:492-496.
49. Van de Peer Y., Maere S., Meyer A. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 2009, 10:725-732.
50. Wada H., Satoh N. Patterning the protochordate neural tube. Curr. Opin. Neurobiol. 2001, 11:16-21.
51. Williams R.W., Herrup K. The control of neuron number. Ann. Rev. Neurosci. 1988, 11:423-453.
52. Yu J.K., Meulemans D., McKeown S.J., Bronner-Fraser M. Insights from the amphioxus genome on the origin of vertebrate neural crest. Genome Res. 2008, 18:1127-1132.
53. Yu J.K., Satou Y., Holland N.D., Shin I.T., Kohara Y., Satoh N., Bronner-Fraser M., Holland L.Z. Axial patterning in cephalochordates and the evolution of the organizer. Nature 2007, 445:613-617.
54. Zhang J. Evolution by gene duplication: an update. Trends Ecol. Evol. 2003, 18:292-298.