Ding Y et al. (2011), Evolution of vertebrate central nervous system ...

XB-ART-44636

J Genet Genomics 2011 Dec 20;3812:577-84. doi: 10.1016/j.jgg.2011.10.004.

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

Chen Y , Ding Y , Zhang Z , Wang W , Chen JY , Ueno N , Mao B .

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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.

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Species referenced: Xenopus laevis
Genes referenced: abi1 abi2 aldoa aldob aldoc arhgef1 arhgef11 arhgef12 atp6v1c1 atp6v1c2 cyria cyrib dkk1 dkk2 eeig1 eeig2 elapor1 elapor2 gab1 gab2 gab3 gnas htra1 htra4 kcnn1 kcnn2 lpcat1 lpcat2 lpcat4 mboat2 ncoa1 ncoa2 ncoa3 nucb1 nucb2 otub1 otub2 pcnx1 pcnx4 pla2g12a pla2g12b ppp3ca prkag1 prkag2 prkag3 pura purb purg rac1 ralgds rcan1 rcan2 rgl2 rgl3 rtn1 rtn2 rtn3 rtn4 samd4a samd4b scrn1 scrn2 scrn3 spred1 spred2 spred3 ssbp1 ssbp2 ssbp3 ssbp4 stau1 stau2 syn1 syn2 syn3 syngr1 syngr2 syngr3 tp63 tprg1 tprg1l usp53 usp54 vps26a vps26b zmym2 zmym3

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	Fig. 1. Strategy to identify duplicated CNS-biased gene families. A: flowchart of the identification of duplicated CNS-biased gene families. B: a phylogenetic tree of a hypothetical gene family. Homo sampies (Hs), Mus musculus (Mm), Xenopus tropicalis (Xt), Ciona intestinalis (Ci), Branchiostoma floridae (Bf), Drosophila melanogaster (Dm) and Nematostella vectensis (Nv). The genes are shown in two clusters. If there are two genes in Ciona, Drosophila or Nematostella in the two clusters but only one in amphioxus, we assume that there is one gene lost in amphioxus.
	Fig. 2. Conserved and non-conserved expression patterns of different gene families in amphioxus and Xenopus. A–F: expression patterns of the “conserved” expressed gene family, RTNs, in Xenopus (A–D) and amphioxus (E, F) larvae. F: the higher magnification of boxed area in E. G–J: expression patterns of the “shifted” expressed gene family, NUCBs, in Xenopus (G, H) and amphioxus (I, J) larvae. K–N: expression patterns of the “expanded” expressed gene family, SAMD4s, in Xenopus (K, L) and amphioxus (M, N) larvae. Scale bars: 1 mm (A–D, G, H, K, L); 100 μm (E, I, M).
	Fig. 3. Origin of vertebrate CNS genes through expression changes of duplicate genes. A: phylogenetic relationships among the species involved in this study. Asterisk denotes the range of the gene duplication we studied. B: tissue distribution of the duplicate gene expression in the CNS of X. laevis. The first column shows the total percentage of CNS-expressed genes. C: a summary of the statistical results of the gene expression patterns. D: diagram shows the possible model for the origination of the CNS-biased genes during the transition from invertebrates to vertebrates. The expression changes of the genes are simplified into two steps.
	Fig. S1. Expression patterns of four conserved expressed gene families: STAU (A–C), FAM49 (D–F), KCNN (G–I) and DKK(J–M). L, M: amphioxus larvae at 24 h and 36 h post-fertilization. Scale bars: 1 mm (A, B, D, E, G, H, J, K); 100 μm (C, F, I, L, M).
	Fig. S2. Expression patterns of three conserved expressed gene families: SYNGR (A–C), TPRG (D–G), PURA (H–J). G: cross section at the position indicated in F, the expression was detected weakly in all the axial structures, mainly in the neural tube (NT) and gut. NC: notochord, SM: somites. Scale bars: 1 mm (A, B, D, E, G, H); 100 μm (C, F, I).
	Fig. S3. Expression patterns of 5 conserved expressed gene families: SYN (A–D), SCRN (E–H), SSBP (I–L), PRKAG (M–P) and ARHGEF (Q–S). Scale bars: 1 mm (A–C, E–G, I–K, M–O, Q–R); 100 μm (D, H, L, P, S).
	Fig. S4. Expression patterns of 4 shifted expressed gene families: UPS53/54 (A–D), ABI (E–H), VPS26 (I–L) and NCOA (M–Q). K: amphioxus larva at 12 h post-fertilization. Q: cross section at the position indicated in P, the expression was detected mainly in the gut (arrowheads). Scale bars: 1 mm (A, B, E, F, I, J, M–O); 100 μm (C, D, G, H, K, L, P).
	Fig. S5. Expression patterns of 3 shifted expressed gene families: APT6V1C (A–D), FAM102 (E–H) and GAB (I–L). C: amphioxus embryos at 12 h post-fertilization. D: amphioxus larva at 24 h post-fertilization. H: cross section at the position indicated in G. G: the expression was detected in the notochord (NC) and gut. Scale bars: 1 mm (A, B, E, F, I–K); 100 μm (C, D, G, L).
	Fig. S6. Expression patterns of 6 expanded expressed gene families: DSCR/RCAN (A–D), OTUB (E–G), RGL (H–K), PCNX (L–O), SPRED (P–S) and ALDO (T–X). C, N: amphioxus embryos at 12 h post-fertilization. W, X: amphioxus larvae at 24 h and 36 h post-fertilization. Scale bars: 1 mm (A, B, E, F, H–J, L, M, P–R, T–V); 100 μm (C, D, G, K, O, S, W, X).Fig. S6. Expression patterns of 6 expanded expressed gene families: DSCR/RCAN (A–D), OTUB (E–G), RGL (H–K), PCNX (L–O), SPRED (P–S) and ALDO (T–X). C, N: amphioxus embryos at 12 h post-fertilization. W, X: amphioxus larvae at 24 h and 36 h post-fertilization. Scale bars: 1 mm (A, B, E, F, H–J, L, M, P–R, T–V); 100 μm (C, D, G, K, O, S, W, X).
	Fig. S7. Expression patterns of the 4 gene families in Xenopus for which no clear expression pattern of their amphioxus homologs were detected. (A–C) LPCAT; (D, E) ZMYM; (F, G) KIAA1324; (H, I) HTRA.
	Fig. S8. RT-PCR analysis of the developmental expression of BbKIAA1324/L, BbLPCAT1/2/4, BbHTRA1/4 and BbZMYM2/3. Bbactin was used as an internal control. NA, negative control without reverse transcriptase in the RT step; 16C, 16-cell stage; GAS, gastrula stage; 12H, 12-hour stage post-fertilization; 24H, 24-hour stage post-fertilization.
	nucb1 (nucleobindin 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	nucb2 (nucleobindin 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	rtn1 (reticulon 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	rtn2 (reticulon 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	rtn4 (reticulon 4) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	samd4a (sterile alpha motif domain containing 4A) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	kcnn1 ( potassium channel, calcium activated intermediate/small conductance subfamily N alpha, member 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	kcnn2 (potassium channel, calcium activated intermediate/small conductance subfamily N alpha, member 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	dkk2 (dickkopf WNT signaling pathway inhibitor 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	cyria (CYFIP related Rac1 interactor A) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	cyrib (CYFIP related Rac1 interactor B) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	stau1 (staufen double-stranded RNA binding protein 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	stau2 (staufen double-stranded RNA binding protein 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	pura (purine-rich element binding protein A) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	purb (purine-rich element binding protein B) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	syngr2 (synaptogyrin 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	tprg1 (tumor protein p63 regulated 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	tprg1L (tumor protein p63 regulated 1-like) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	arhgef11(Rho guanine nucleotide exchange factor 11) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	arhgef12 (Rho guanine nucleotide exchange factor 12) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	prkag2 (protein kinase, AMP-activated, gamma 2 non-catalytic subunit) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	prkag1 (protein kinase, AMP-activated, gamma 1 non-catalytic subunit) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	prkag3 (protein kinase, AMP-activated, gamma 3 non-catalytic subunit) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	scrn1 (secernin 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	scrn2 (secernin 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	scrn3 (secernin 3) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	ssbp2 (single-stranded DNA binding protein 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	ssbp3 (single-stranded DNA binding protein 3) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	ssbp4 (single-stranded DNA binding protein 4) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	syn1 (synapsin I) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	syn2 (synapsin II) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	syn3 (synapsin III) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	abi1 (abl interactor 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	abi2 (abl interactor 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	ncoa1 (nuclear receptor coactivator 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	ncoa2 (nuclear receptor coactivator 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	ncoa3 (nuclear receptor coactivator 3) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	usp53 (ubiquitin specific peptidase 53) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	usp54 (ubiquitin specific peptidase 54) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	vps26a (VPS26 retromer complex component A) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	vps26b (VPS26 retromer complex component B) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	atp6v1c1 (ATPase, H+ transporting, lysosomal 42kDa, V1 subunit C1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	atp6v1c2(ATPase, H+ transporting, lysosomal 42kDa, V1 subunit C2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	eeig1 (EEIG family member 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	eeig2 (EEIG family member 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	gab1 (GRB2 associated binding protein 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	gab2 (GRB2 associated binding protein 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	gab3 (GRB2 associated binding protein 3) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	otub1 (OTU deubiquitinase, ubiquitin aldehyde binding 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	otub2 (OTU deubiquitinase, ubiquitin aldehyde binding 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	pcnx1 (pecanex homolog 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	pcnx4 (pecanex homolog 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	ralgds (ral guanine nucleotide dissociation stimulator) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	rcan1 (regulator of calcineurin 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	rcan2 (regulator of calcineurin 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	rgl2 (ral guanine nucleotide dissociation stimulator-like 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	rgl3 (ral guanine nucleotide dissociation stimulator-like 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	spred1 (sprouty-related, EVH1 domain containing 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	spred3 (sprouty-related, EVH1 domain containing 3) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	htra4 (HtrA serine peptidase 4) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	elapor1 (endosome-lysosome associated apoptosis and autophagy regulator 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	lpcat1 (lysophosphatidylcholine acyltransferase 1) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	lpcat2 (lysophosphatidylcholine acyltransferase 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	lpcat4 (lysophosphatidylcholine acyltransferase 4) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	zmym2 (zinc finger, MYM-type 2) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.
	zmym3 (zinc finger, MYM-type 3) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 32, lateral view, anterior left, dorsal up.