XB-ART-55870
Dev Genes Evol
January 1, 2019;
229
(2-3):
53-72.
Transcriptome profiling reveals male- and female-specific gene expression pattern and novel gene candidates for the control of sex determination and gonad development in Xenopus laevis.
Abstract
Xenopus laevis is an amphibian (frog) species widely used in developmental biology and genetics. To unravel the molecular machinery regulating sex differentiation of Xenopus gonads, we analyzed for the first time the transcriptome of developing amphibian gonads covering sex determination period. We applied microarray at four developmental stages: (i) NF50 (undifferentiated
gonad during sex determination), (ii) NF53 (the onset of sexual differentiation of the gonads), (iii) NF56 (sexual differentiation of the gonads), and (iv) NF62 (developmental progression of differentiated gonads). Our analysis showed that during the NF50, the genetic female (ZW) gonads expressed more sex-specific genes than genetic male (ZZ) gonads, which suggests that a robust genetic program is realized during female sex determination in Xenopus. However, a contrasting expression pattern was observed at later stages (NF56 and NF62), when the ZW gonads expressed less sex-specific genes than ZZ gonads, i.e., more genes may be involved in further development of the male gonads (ZZ). We identified sexual dimorphism in the expression of several functional groups of genes, including signaling factors, proteases, protease inhibitors, transcription factors, extracellular matrix components, extracellular matrix enzymes, cell adhesion molecules, and
epithelium-specific intermediate filaments. In addition, our analysis detected a sexually dimorphic expression of many uncharacterized genes of unknown function, which should be studied further to reveal their identity and if/how they regulate
gonad development, sex determination, and sexual differentiation. Comparison between genes sex-specifically expressed in developing gonads of Xenopus and available transcriptome data from zebrafish, two reptile species, chicken, and mouse revealed significant differences in the genetic control of sex determination and
gonad development. This shows that the genetic control of
gonad development is evolutionarily malleable.
PubMed ID:
30972573
PMC ID:
PMC6500517
Article link:
Dev Genes Evol
Grant support:
[+]
DEC-2013/11/D/NZ3/00184 Narodowe Centrum Nauki
Species referenced:
Xenopus laevis
Genes referenced:
adam21
alb
aldh3b1
alox12b
anxa13
avil
bcan
birc5
cadm3
capn8.1
ccdc50
cdh26
cela1.1
cela1.5
chrd.1
cldn6.1
col1a1
col2a1
col3a1
col9a1
col9a3
crabp2
ctsh
ctsk
ctsl
cx38
dcn
ddx25
dhh
dmrt2
dppa2
emx1
esr1
esr2
fbn3
fetub
fgfbp1
fgfr4
foxa2
foxf1
foxh1
foxo1
foxr1
fzd10
fzd4
gata2
gde1
gdf1
gdf3
gja3
hoxa9
hoxd10
hoxd13
hrg
hspb6
igf1
igf3
igfbp1
ihh
isyna1
itga11
jak2
kdm6b
klf15
klf9
kpna2
krt12.1
krt15.1
krt19
krt78.2
lhx1
lhx8
lum
mafb
matn2
matn4
mmp1
mmp11
mmp16
mmp2
mmp28
mmp7
mogat2.1
nes
ngfr
ocln
ocm4.3
ocm4.5
pabpn1l
pcsk6
pou5f3.3
prss1
prss3
ptger3
ptx
racgap1
rbm20
rbp2
rbp4
rdh16
rnf138
sag
sdf2l1
serpina1
serpina3
serpinc1
serpinf2
serpini2
sh3glb2
shh
smad4
sncg
spdyc
srpx2
sycp3
tfip11
timp2
timp3
twist1
vegt
velo1
vill
vtn
vwa2
wnt10b
wnt11
wnt11b
wnt3a
wnt7b
wnt8b
XB5745823 [provisional]
zar1
zp2
zp3
zp4
zpd
zpy1
GO keywords:
sex determination
[+]
GEO Series:
GSE105103:
NCBI
Article Images:
[+] show captions
|
Fig. 1. Structural changes in developing gonads. a, b At stage NF50, there is no difference in the gonad structure between genetic sexes (ZW and ZZ). Such undifferentiated gonads (arrows) are composed of the somatic cells of coelomic epithelium (ce) covering the gonad, and germ cells (g) located inside; the germ cells are attached to the coelomic epithelium. The somatic cells gather in the gonad center forming gonadal medulla (m). At stage NF53, the first sexual differences appear in the gonad structure; in the differentiating ovaries (c, ZW), the germ cells remain in the peripheral position forming the ovarian cortex, whereas the centrally located medulla remains sterile. In the ZZ (male) gonads at the onset of sexual differentiation (d, the onset of the testis differentiation), the germ cells (g) detach from the coelomic epithelium and move towards the gonad center (medulla, m). At stage NF56, the differentiating ovaries (e) becomes compartmentalized into cortex and medulla; all germ cells (g) are located in the cortex and are attached to the coelomic epithelium; an ovarian cavity forms in the medulla (asterisk). In the differentiating testes (f), the germ cells (g) are dispersed and the cortex and medulla are absent. At stage NF62, the ovaries (g) contain large ovarian cavity (asterisk); the ovarian cortex contains meiotic cells (o). In the testes (h), the germ cells (g) are located within the testis cords (encircled). Scale bar, 25 μm
|
|
Fig. 2 Diagram of changes in the number of genes upregulated and downregulated (≥ 2-fold change) between different stages in ZW gonads (a) and ZZ gonads (b)
|
|
Fig. 3. Diagram of changes in the number of genes with higher expression in ZW or ZZ gonads (≥ 2-fold change).
|
|
Fig. 4. Subcellular distribution of gene products (obtained from the Ingenuity Pathway Analysis).
|
References [+] :
Ayers,
Identification of candidate gonadal sex differentiation genes in the chicken embryo using RNA-seq.
2016,
Pubmed
Ayers,
Identification of candidate gonadal sex differentiation genes in the chicken embryo using RNA-seq.
2016,
Pubmed
Bachiller,
The organizer factors Chordin and Noggin are required for mouse forebrain development.
2000,
Pubmed
Bar,
Transcriptome analysis reveals differentially expressed genes associated with germ cell and gonad development in the Southern bluefin tuna (Thunnus maccoyii).
2016,
Pubmed
Beverdam,
Expression profiling of purified mouse gonadal somatic cells during the critical time window of sex determination reveals novel candidate genes for human sexual dysgenesis syndromes.
2006,
Pubmed
Chen,
Identification of novel markers of mouse fetal ovary development.
2012,
Pubmed
Czerwinski,
A timecourse analysis of systemic and gonadal effects of temperature on sexual development of the red-eared slider turtle Trachemys scripta elegans.
2017,
Pubmed
Gong,
Transcriptome profiling of the developing postnatal mouse testis using next-generation sequencing.
2013,
Pubmed
Haselman,
Global gene expression during early differentiation of Xenopus (Silurana) tropicalis gonad tissues.
2015,
Pubmed
,
Xenbase
Jameson,
Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad.
2012,
Pubmed
Nef,
Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development.
2006,
Pubmed
Ogunyemi,
Differentially expressed genes in adipocytokine signaling pathway of adipose tissue in pregnancy.
2019,
Pubmed
Pappano,
Coding sequence and expression patterns of mouse chordin and mapping of the cognate mouse chrd and human CHRD genes.
1998,
Pubmed
Piprek,
Transcriptome analysis identifies genes involved in sex determination and development of Xenopus laevis gonads.
2018,
Pubmed
,
Xenbase
Piprek,
Development of Xenopus laevis bipotential gonads into testis or ovary is driven by sex-specific cell-cell interactions, proliferation rate, cell migration and deposition of extracellular matrix.
2017,
Pubmed
,
Xenbase
Piprek,
Early Development of the Gonads: Origin and Differentiation of the Somatic Cells of the Genital Ridges.
2017,
Pubmed
Piprek,
Differential effects of busulfan on gonadal development in five divergent anuran species.
2013,
Pubmed
,
Xenbase
Sasai,
Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes.
1995,
Pubmed
,
Xenbase
Scheider,
Gene expression of chicken gonads is sex- and side-specific.
2015,
Pubmed
Small,
Profiling gene expression during the differentiation and development of the murine embryonic gonad.
2005,
Pubmed
Sreenivasan,
Transcriptomic analyses reveal novel genes with sexually dimorphic expression in the zebrafish gonad and brain.
2008,
Pubmed
Sun,
Gonad Transcriptome Analysis of High-Temperature-Treated Females and High-Temperature-Induced Sex-Reversed Neomales in Nile Tilapia.
2018,
Pubmed
Toker,
The biology and biochemistry of diacylglycerol signalling. Meeting on molecular advances in diacylglycerol signalling.
2005,
Pubmed
Tsukiyama,
Ymer acts as a multifunctional regulator in nuclear factor-κB and Fas signaling pathways.
2012,
Pubmed
Xu,
The testis and ovary transcriptomes of the rock bream (Oplegnathus fasciatus): A bony fish with a unique neo Y chromosome.
2016,
Pubmed
Yatsu,
RNA-seq analysis of the gonadal transcriptome during Alligator mississippiensis temperature-dependent sex determination and differentiation.
2016,
Pubmed
Yoshimoto,
Opposite roles of DMRT1 and its W-linked paralogue, DM-W, in sexual dimorphism of Xenopus laevis: implications of a ZZ/ZW-type sex-determining system.
2010,
Pubmed
,
Xenbase
Yoshimoto,
A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis.
2008,
Pubmed
,
Xenbase
