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Transcriptomic study of the sex differentiation process in turbot

ABSTRACT: Gonad is a bipotential tissue that depending on the genetic and environmental inputs its final phenotype will be determined. Gonadal development is a very complex process because from an undifferentiated gonad the future testis or ovary will be formed. To better understand the complexity of the gonad plasticity throughout development we explored the transcriptomic landscape of gonads from undifferentiated to juvenile fish. For this study we have used turbot (Scophthalmus maximus) that presents one of the most remarkable sexual dimorphism in cultured fish species. With the aim of identifying gene patterns for each gonad developmental stages a microarray species-specific enriched by reproduction- and immune-related genes was assessed. Further genes with sex-differential mRNA expression were mapped in the sex- and growth-QTL (quantitative trait loci) markers. Data revealed that gonadal transcriptome prevail in front of fish biometry as it was possible to classify gonads according to sexual development status by using gene expression profiles rather than their age or size. The same classification was observed with a selection of a subset of reproduction-related genes showing the importance of gene profiles for each of the developing gonadal stage. Overall microarray data showed the importance of the level of expression (intensity) rather than the number of genes found in each development period. Larger numbers of differentially expressed genes (DEG) were found in the differentiating gonads when compared to ovaries and much smaller number resulted when compared to testis. However, more number of DEG was found in testis when compared to ovaries. The earliest presence of cyp19a1a, the key female sex differentiation gene, was found at 90 dpf together with its transcription factor foxl2 showing at the same time a positive correlation with other genes related to extracellular matrix (ecm2), immune system (irf5) or methylation (sall1). The presence of male-related genes like sox9 was evidenced at early developmental stages (70 and 90 dpf) while expression of dmrt3 started not earlier than 150 dpf, coinciding when larger number of male-related genes were found. All developmental stages presented genes related to immune system and epigenetic mechanisms revealing their importance during gonadal development. Sex-QTLs showed larger amount of sex-differential transcripts in the linkage group 6 and 21 both in males and females but transcripts mapped near growth-QTLs were only found in females. Here it is presented the first assessment of the expression profiles observed in the gonads at different developmental stages by identifying genes responsible for male or female traits. It has been identified gene clusters for each developmental stages and gene network interactions for each sexual phenotype. The expression of known male and female-related genes were precisely described throughout gonadal development as well as the expression of other genes with an unknown reproduction function which have been identified for the first time during sexual development process. In addition, it was possible to localize some of these genes on the sex- and growth-QTLs. The data presented here can help to better understand the reproduction system in cultured fish species and improved selection breeding programs to increase their productivity.

ORGANISM(S): Scophthalmus maximus

PROVIDER: GSE64280 | GEO | 2016/05/20

SECONDARY ACCESSION(S): PRJNA270628

REPOSITORIES: GEO

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Project description:Gonadal sex differentiation – testis versus ovary formation – is a fundamental process required for reproduction and evolution. Reflecting this importance, the embryonic gonads of vertebrate species comprise the same key cell types; germ cells, supporting cells and interstitial steroidogenic cells. Remarkably, the genetic triggers for gonadal sex differentiation vary across species (the SRY gene in mammals, DMRT1 in birds and some turtles, temperature in many reptiles, AMH and various other genes in fishes). Despite this variation, the cell biology of gonadal development was long thought to be largely conserved. Here, we present a comprehensive analysis of gonadal sex differentiation, using the chicken embryo as a model and considering the entire gonad. We sampled over 30,000 cells across several developmental stages, prior, during and after the onset of gonadal sex differentiation. The data provide several new insights into cell lineage specification during vertebrate gonadogenesis. Combining lineage tracing with single cell transcriptomics, the data show that somatic supporting cells of the embryonic chicken gonad do not derive from the coelomic epithelium, in contrast to other vertebrates studied. Instead, the early somatic precursors cells of the gonads in both sexes derive from a DMRT1+/PAX2+/WNT4+/OSR1+ mesenchymal cell population. In particular, PAX2 marks immigrating mesenchymal cells that give rise to the supporting cell lineage. We find a greater complexity of gonadal cell types than previously thought, including the identification of two distinct sub-populations of Sertoli cells in developing testes, and derivation of embryonic steroidogenic cells from a differentiated supporting cell lineage. We provide significantly improved resolution of gonadal cell types and identify several new gonadal marker genes. Altogether, these results indicate that, just as the genetic trigger for sex differs across vertebrate groups, cell lineage specification in the gonad may also vary substantially.

Project description:Abstract. The molecular pathways in embryonic vertebrates leading to gonad formation in each sex are incompletely understood. The purpose of this study was to identify novel genes that could be associated with sex-specific gonadal differentiation in a fish, the rainbow trout (Oncorhynchus mykiss). This study was facilitated by a custom microarray based on 7,681 genes derived from embryonic rainbow trout gonad cDNA libraries and public databases. Gonad samples for total RNA isolation were obtained from pvasa-green fluorescent protein (pvasa-GFP) transgenic rainbow between 300 and 700 degree days of development post-fertilization. The transgenic fish permitted the collection of gonads from embryonic rainbow trout during the period of molecular sex differentiation in advance of any morphologically distinguishable characteristics of sex. A bioinformatic method was used with the microarray data that looked for strong associations in gene expression patterns between known sex differentiation genes (the target genes) and novel genes (the target-associated genes) previously not allied with sex differentiation in fishes. The expression patterns of representative targets genes from both sexes and their target-associated genes were independently confirmed by real-time reverse transcription-polymerase chain reaction to support the validity of the bioinformatics method employed. Numerous, novel genes were identified in the gonads of embryonic female and male rainbow trout that could be involved in sex-specific differentiation pathways in this fish. Embryonic gonads were removed by dissection from known genetic female (XX) and male (XY) rainbow trout (Oncorhynchus mykiss) from a transgenic population where expression of GFP is controlled by vasa-gene regulatory elements (Yoshizaki et al. 2000; Takeuchi et al. 2002). These fish were maintained in incubators containing flowing freshwater (10Â°C) at the Ooizumi Research Station, Yamanashi, Japan. Ten female or male transgenic rainbow trout were randomly selected every 5 days, beginning at 30 days (i.e., 300 degree days = incubation temperature in Â°C x number of days) post fertilization through until 70 days (i.e., 700 degree days) post fertilization. The gonads from each sex, at each sampling time, were pooled and immediately frozen for subsequent total RNA isolation.

Project description:Background: Sex in fish is plastic and in several species can be influenced by environmental factors. In sensitive species, elevated temperatures have a masculinizing effect. Previous studies on the effects of temperature on gene expression have been restricted to a few cognate genes, mostly related to testis or ovarian development, and analyzed in gonads once they had completed the process of sex differentiation. However, studies on the effect of temperature at the whole gonadal transcriptomic level are scarce in fish and, in addition, temperature effects at the time of sex differentiation at the transcriptomic level are also unknown. Here, we used the European sea bass, a gonochoristic teleost with a polygenic sex determination system influenced by temperature, and exposed larvae to elevated temperature during the period of early gonad formation. Transcriptomic analysis of the gonads was carried out about three months after the end of temperature exposure, shortly after the beginning of the process of sex differentiation. Results: Elevated temperature doubled the number of males with respect to untreated controls. Transcriptomic analysis of early differentiating female gonads showed how heat caused: 1) an up-regulation of genes related to cholesterol transport (star), the stress response (nr3c1) and testis differentiation (amh, dmrt, etc.), 2) a decrease in the expression of genes related to ovarian differentiation such as cyp19a1a, and 3) an increase in the expression of several genes related to epigenetic regulatory mechanisms (hdac11, dicer1, ehmt2, jarid2a, pcgf2, suz12, mettl22). Conclusions: Taken together, the results of this study contribute to the understanding of how the early environment sets permanent changes that result in long-lasting consequences, in this case in the sexual phenotype. Results also show the usefulness of comparing the effects of heat on the behavior of cognate genes related to sex differentiation as well as that of genes involved in establishing and maintaining cell identity through epigenetic mechanisms.

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Transcriptomic study of the sex differentiation process in turbot

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