PUBLICATION

Fibroblast growth factor signaling is required for early somatic gonad development in zebrafish

Authors

Leerberg, D.M., Sano, K., Draper, B.W.

ID

ZDB-PUB-170906-1

Date

2017

Source

PLoS Genetics 13: e1006993 (Journal)

Registered Authors

Draper, Bruce, Leerberg, Dena M.

Keywords

Gonads, Germ cells, Zebrafish, Fibroblast growth factor, Gene expression, Developmental signaling, Testes, Vertebrates

MeSH Terms

Animals
Embryonic Development/genetics
Female
Fibroblast Growth Factors/genetics*
Gene Expression Regulation, Developmental
Gonads/growth & development*
Male
Morphogenesis/genetics*
Ovary/growth & development
Ovary/metabolism
Sex Differentiation/genetics
Signal Transduction
Testis/growth & development
Testis/metabolism
Zebrafish/genetics
Zebrafish/growth & development*
Zebrafish Proteins/genetics*

(all 17)

PubMed

28873404 Full text @ PLoS Genet.

Abstract

The vertebrate ovary and testis develop from a sexually indifferent gonad. During early development of the organism, primordial germ cells (the gamete lineage) and somatic gonad cells coalesce and begin to undergo growth and morphogenesis to form this bipotential gonad. Although this aspect of development is requisite for a fertile adult, little is known about the genetic regulation of early gonadogenesis in any vertebrate. Here, we provide evidence that fibroblast growth factor (Fgf) signaling is required for the early growth phase of a vertebrate bipotential gonad. Based on mutational analysis in zebrafish, we show that the Fgf ligand 24 (Fgf24) is required for proliferation, differentiation, and morphogenesis of the early somatic gonad, and as a result, most fgf24 mutants are sterile as adults. Additionally, we describe the ultrastructural elements of the early zebrafish gonad and show that distinct somatic cell populations can be identified soon after the gonad forms. Specifically, we show that fgf24 is expressed in an epithelial population of early somatic gonad cells that surrounds an inner population of mesenchymal somatic gonad cells that are in direct contact with the germ cells, and that fgf24 is required for stratification of the somatic tissue. Furthermore, based on gene expression analysis, we find that differentiation of the inner mesenchymal somatic gonad cells into functional cell types in the larval and early juvenile-stage gonad is dependent on Fgf24 signaling. Finally, we argue that the role of Fgf24 in zebrafish is functionally analogous to the role of tetrapod FGF9 in early gonad development.

Genes / Markers

Marker	Marker Type	Name
amh	GENE	anti-Mullerian hormone
cyp19a1a	GENE	cytochrome P450, family 19, subfamily A, polypeptide 1a
ddx4	GENE	DEAD (Asp-Glu-Ala-Asp) box polypeptide 4
etv4	GENE	ETS variant transcription factor 4
fgf24	GENE	fibroblast growth factor 24
gata4	GENE	GATA binding protein 4
gsdf	GENE	gonadal somatic cell derived factor
nr5a1a	GENE	nuclear receptor subfamily 5, group A, member 1a
tp53	GENE	tumor protein p53
wt1a	GENE	WT1 transcription factor a

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Figures

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Expression

Gene	Antibody	Fish	Conditions	Stage	Anatomy	Assay	Figure
amh		AB	standard conditions	Days 7-13	gonad primordium somatic cell	ISH	Fig. 5
amh		fgf24^uc47/uc47 (AB)	standard conditions	Days 7-13	gonad primordium somatic cell	ISH	Fig. 5
cyp19a1a		AB	standard conditions	Days 7-13	gonad primordium somatic cell	ISH	Fig. 5
cyp19a1a		fgf24^uc47/uc47 (AB)	standard conditions	Days 7-13	gonad primordium somatic cell	ISH	Fig. 5
ddx4	ab1-ddx4	AB	standard conditions	Days 7-13	germ line cell	IHC	Fig. 5
ddx4	ab1-ddx4	AB	standard conditions	Days 7-13	germ line cell	IHC	Fig. 4
ddx4	ab1-ddx4	AB	standard conditions	Days 7-13	gonad primordium germ line cell	IHC	Fig. 8
ddx4	ab1-ddx4	AB	standard conditions	Days 7-13	gonad primordium germ line cell	IHC	Fig. 7
ddx4	ab1-ddx4	AB	standard conditions	Days 7-13	gonad primordium germ line cell	IHC	Fig. 2
ddx4	ab1-ddx4	AB	standard conditions	Days 14-20	immature gonad germ line cell	IHC	Fig. 2

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Phenotype

Fish	Conditions	Stage	Phenotype	Figure
fgf24^{t22030/t22030}	standard conditions	Days 7-13	germ line cell decreased amount, abnormal	Fig. 2
fgf24^{t22030/t22030}	standard conditions	Days 7-13	gonad primordium decreased size, abnormal	Fig. 2
fgf24^{t22030/t22030}	standard conditions	Days 14-20	germ line cell decreased amount, abnormal	Fig. 2
fgf24^{t22030/t22030}	standard conditions	Adult	female organism absent, abnormal	Fig. 2
fgf24^{t22030/t22030}	standard conditions	Adult	whole organism lacks all parts of type pectoral fin, abnormal	Fig. 2
fgf24^uc47/uc47 (AB)	standard conditions	Days 7-13	gonad primordium ab1-lama1 labeling absent, abnormal	Fig. 7
fgf24^uc47/uc47 (AB)	standard conditions	Days 7-13	gonad primordium germ line cell ddx4 expression decreased amount, abnormal	Fig. 2
fgf24^uc47/uc47 (AB)	standard conditions	Days 7-13	gonad primordium germ line cell ab1-ctnnb labeling decreased amount, abnormal	Fig. 8
fgf24^uc47/uc47 (AB)	standard conditions	Days 7-13	gonad primordium somatic cell amh expression decreased amount, abnormal	Fig. 5
fgf24^uc47/uc47 (AB)	standard conditions	Days 7-13	gonad primordium somatic cell cyp19a1a expression decreased amount, abnormal	Fig. 5

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Mutations / Transgenics

Allele	Construct	Type	Affected Genomic Region
t22030		Point Mutation	fgf24
uc02Tg	Tg(piwil1:EGFP)	Transgenic Insertion
uc46Tg	Tg(gsdf:mCherry)	Transgenic Insertion
uc47		Insertion	fgf24
zdf1		Point Mutation	tp53

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Human Disease / Model

Sequence Targeting Reagents

Target	Reagent	Reagent Type
fgf24	CRISPR1-fgf24	CRISPR

Fish

Fish
AB
fgf24^{t22030/t22030}
fgf24^uc47/uc47 (AB)
fgf24^uc47/uc47; uc02Tg
fgf24^uc47/uc47; uc02Tg; uc46Tg
tp53^zdf1/zdf1; fgf24^uc47/uc47
uc02Tg
uc02Tg; uc46Tg
uc46Tg

Antibodies

Orthology

Engineered Foreign Genes

Marker	Marker Type	Name
EGFP	EFG	EGFP
mCherry	EFG	mCherry

Mapping

Leerberg et al., 2017 ZDB-PUB-170906-1 PMID:28873404

Fibroblast growth factor signaling is required for early somatic gonad development in zebrafish

Leerberg et al., 2017

ZDB-PUB-170906-1
PMID:28873404