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

Yuan Chen; Yun Ding; Zuming Zhang; Wen Wang; Jun-Yuan Chen; Naoto Ueno; Bingyu Mao

doi:10.1016/j.jgg.2011.10.004

Volume 38 Issue 12

Dec. 2011

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

doi: 10.1016/j.jgg.2011.10.004

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

a
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Jiaochang East Road 32, Kunming 650223, China
b
Graduate University of Chinese Academy of Sciences, Beijing 100049, China
c
School of Life Sciences, Nanjing University, Hankou Road, Nanjing, Jiangsu 210093, China
d
Division of Morphogenesis, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki, Aichi 444-8585, Japan

More Information

Corresponding author: E-mail address: mao@mail.kiz.ac.cn (Bingyu Mao)
Received Date: 2011-09-15
Accepted Date: 2011-10-18
Rev Recd Date: 2011-10-17

Available Online: 2011-12-03

Publish Date: 2011-12-20

Abstract

Abstract

The evolution of the central nervous system (CNS) is one of the most striking changes during the transition from invertebrates to vertebrates. As a major source of genetic novelties, gene duplication might play an important role in the functional innovation of vertebrate CNS. In this study, we focused on a group of CNS-biased genes that duplicated during early vertebrate evolution. We investigated the tempo-spatial expression patterns of 33 duplicate gene families and their orthologs during the embryonic development of the vertebrate Xenopus laevis and the cephalochordate Brachiostoma belcheri. Almost all the identified duplicate genes are differentially expressed in the CNS in Xenopus embryos, and more than 50% and 30% duplicate genes are expressed in the telencephalon and mid-hindbrain boundary, respectively, which are mostly considered as two innovations in the vertebrate CNS. Interestingly, more than 50% of the amphioxus orthologs do not show apparent expression in the CNS in amphioxus embryos as detected by in situ hybridization, indicating that some of the vertebrate CNS-biased duplicate genes might arise from non-CNS genes in invertebrates. Our data accentuate the functional contribution of gene duplication in the CNS evolution of vertebrate and uncover an invertebrate non-CNS history for some vertebrate CNS-biased duplicate genes.
- Central nervous system evolution,
- Gene duplication,
- Expression pattern,
- Amphioxus

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References(54)

References

[1]	Altschul, S.F., Gish, W., Miller, W. et al. Basic local alignment search tool J. Mol. Biol., 215 (1990),pp. 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., 280 (2005),pp. 43131-43140
[3]	Carroll, S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution Cell, 134 (2008),pp. 25-36
[4]	Carroll, S.B., Grenier, J.K., Weatherbee, S.D.
[5]	Castro, L.F., Rasmussen, S.L., Holland, P.W. et al. A Gbx homeobox gene in amphioxus: insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary Dev. Biol., 295 (2006),pp. 40-51
[6]	Catchen, J.M., Conery, J.S., Postlethwait, J.H. Automated identification of conserved synteny after whole-genome duplication Genome Res., 19 (2009),pp. 1497-1505
[7]	Chen, J.Y. Early crest animals and the insight they provide into the evolutionary origin of craniates Genesis, 46 (2008),pp. 623-639
[8]	Davidson, E.H., Erwin, D.H. Gene regulatory networks and the evolution of animal body plans Science, 311 (2006),pp. 796-800
[9]	de Martino, S., Yan, Y.L., Jowett, T. et al. Dev. Dyn., 217 (2000),pp. 279-292
[10]	Dehal, P., Boore, J.L. Two rounds of whole genome duplication in the ancestral vertebrate PLoS Biol., 3 (2005),p. e314
[11]	Delsuc, F., Brinkmann, H., Chourrout, D. et al. Tunicates and not cephalochordates are the closest living relatives of vertebrates Nature, 439 (2006),pp. 965-968
[12]	Donoghue, P.C., Purnell, M.A. Genome duplication, extinction and vertebrate evolution Trends Ecol. Evol., 20 (2005),pp. 312-319
[13]	Gawantka, V., Delius, H., Hirschfeld, K. et al. EMBO J., 14 (1995),pp. 6268-6279
[14]	Glardon, S., Holland, L.Z., Gehring, W.J. et al. Development, 125 (1998),pp. 2701-2710
[15]	Glinka, A., Wu, W., Delius, H. et al. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction Nature, 391 (1998),pp. 357-362
[16]	Harris, C.D., Ermak, G., Davies, K.J. Cell Mol. Life Sci., 62 (2005),pp. 2477-2486
[17]	Holland, L.Z., Holland, N.D. Chordate origins of the vertebrate central nervous system Curr. Opin. Neurobiol., 9 (1999),pp. 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., 72 (2008),pp. 91-105
[19]	Holland, L.Z., Laudet, V., Schubert, M. The chordate amphioxus: an emerging model organism for developmental biology Cell Mol. Life Sci., 61 (2004),pp. 2290-2308
[20]	Holland, L.Z., Albalat, R., Azumi, K. et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology Genome Res., 18 (2008),pp. 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, 23 (2001),pp. 142-151
[22]	Holland, P.W. Methods Mol. Biol., 97 (1999),pp. 641-644
[23]	Holland, P.W., Garcia-Fernandez, J., Williams, N.A. et al. Gene duplications and the origins of vertebrate development Dev. Suppl. 1994 (1994),pp. 125-133
[24]	Hughes, A.L. The evolution of functionally novel proteins after gene duplication Proc. Biol. Sci., 256 (1994),pp. 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, 2 (2002),pp. 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., 306 (2006),pp. 470-480
[27]	Jeffery, W.R., Strickler, A.G., Yamamoto, Y. Migratory neural crest-like cells form body pigmentation in a urochordate embryo Nature, 431 (2004),pp. 696-699
[28]	Jeffery, W.R., Chiba, T., Krajka, F.R. et al. Dev. Biol., 324 (2008),pp. 152-160
[29]	Kasahara, M. The 2R hypothesis: an update Curr. Opin. Immunol., 19 (2007),pp. 547-552
[30]	Kohler, M., Hirschberg, B., Bond, C.T. et al. Small-conductance, calcium-activated potassium channels from mammalian brain Science, 273 (1996),pp. 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., 53 (2009),pp. 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., 23 (2006),pp. 1119-1128
[33]	Lynch, M., Conery, J.S. The evolutionary fate and consequences of duplicate genes Science, 290 (2000),pp. 1151-1155
[34]	Meulemans, D., Bronner-Fraser, M. Insights from amphioxus into the evolution of vertebrate cartilage PLoS ONE, 2 (2007),p. 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., 11 (1999),pp. 699-704
[36]	Morel, N. Neurotransmitter release: the dark side of the vacuolar-H+ATPase Biol. Cell, 95 (2003),pp. 453-457
[37]	Ohno, S.
[38]	Pietri, T., Easley-Neal, C., Wilson, C. et al. Six cadm/SynCAM genes are expressed in the nervous system of developing zebrafish Dev. Dyn., 237 (2008),pp. 233-246
[39]	Putnam, N.H., Butts, T., Ferrier, D.E. et al. The amphioxus genome and the evolution of the chordate karyotype Nature, 453 (2008),pp. 1064-1071
[40]	Rosahl, T.W., Spillane, D., Missler, M. et al. Essential functions of synapsins I and II in synaptic vesicle regulation Nature, 375 (1995),pp. 488-493
[41]	Schubert, M., Escriva, H., Xavier-Neto, J. et al. Amphioxus and tunicates as evolutionary model systems Trends Ecol. Evol., 21 (2006),pp. 269-277
[42]	Semon, M., Wolfe, K.H. Consequences of genome duplication Curr. Opin. Genet. Dev., 17 (2007),pp. 505-512
[43]	Stansberg, C., Vik-Mo, A.O., Holdhus, R. et al. Gene expression profiles in rat brain disclose CNS signature genes and regional patterns of functional specialisation BMC Genomics, 8 (2007),p. 94
[44]	Su, A., Wiltshire, T., Batalov, S. et al. A gene atlas of the mouse and human protein-encoding transcriptomes Proc. Natl. Acad. Sci. USA, 101 (2004),p. 6062
[45]	Takahashi, T. The evolutionary origins of vertebrate midbrain and MHB: insights from mouse, amphioxus and ascidian Dmbx homeobox genes Brain Res. Bull., 66 (2005),pp. 510-517
[46]	Tamura, K., Dudley, J., Nei, M. et al. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0 Mol. Biol. Evol., 24 (2007),pp. 1596-1599
[47]	Tatusov, R.L., Koonin, E.V., Lipman, D.J. A genomic perspective on protein families Science, 278 (1997),pp. 631-637
[48]	Teichmann, S.A., Babu, M.M. Gene regulatory network growth by duplication Nat. Genet., 36 (2004),pp. 492-496
[49]	Van de Peer, Y., Maere, S., Meyer, A. The evolutionary significance of ancient genome duplications Nat. Rev. Genet., 10 (2009),pp. 725-732
[50]	Wada, H., Satoh, N. Patterning the protochordate neural tube Curr. Opin. Neurobiol., 11 (2001),pp. 16-21
[51]	Williams, R.W., Herrup, K. The control of neuron number Ann. Rev. Neurosci., 11 (1988),pp. 423-453
[52]	Yu, J.K., Meulemans, D., McKeown, S.J. et al. Insights from the amphioxus genome on the origin of vertebrate neural crest Genome Res., 18 (2008),pp. 1127-1132
[53]	Yu, J.K., Satou, Y., Holland, N.D. et al. Axial patterning in cephalochordates and the evolution of the organizer Nature, 445 (2007),pp. 613-617
[54]	Zhang, J. Evolution by gene duplication: an update Trends Ecol. Evol., 18 (2003),pp. 292-298