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Persistent epigenetics changes due to elevated temperature during early development in mature zebrafish gonads

ABSTRACT: Sexual development is a process regulated by complex interactions of molecular events that define the final sexual phenotype. Although the genetic and transcriptomic mechanisms involved in the formation of an ovary or a testis are largely studied, the epigenetic mechanisms regulating the fate of an undifferentiated gonad remain poorly understood. Using the zebrafish model (Danio rerio), we exposed larvae of two independent families to high temperature during sex differentiation (18-32 days post fertilization), and by a targeted sequencing approach, we analyzed the methylation profiles of 18 genes related to sexual development in mature gonads two months after the exposure. Gene expression patterns were measured by qPCR in order to correlate them with the DNA methylation. Methylation profiles were family-dependent. However, general patterns of sexual dimorphism were observed in the DNA methylation levels of steroidogenic enzymes (e.g. cyp19a1a, hsd17b1 and hsd11b2), transcription factors (e.g. dmrt1 and amh) and epigenetic-related (dnmt1) genes. In testes, temperature was able to alter the methylation levels of some genes by hypermethylation (cyp19a1a, cyp11a1, amh) or hypomethylation (dmrt1), whereas in ovaries, no changes in the methylation levels were observed. Our results indicate that high temperature during sex differentiation altered methylation in the adult fish gonads and as a novelty, methylation patterns of some genes (e.g., cyp11c1, hsd11b2, dmrt3a and ar) were described here for the fish time in fish.

ORGANISM(S): Danio rerio

PROVIDER: GSE133088 | GEO | 2022/05/20

REPOSITORIES: GEO

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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.

Project description: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.

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Persistent epigenetics changes due to elevated temperature during early development in mature zebrafish gonads

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