Abstract
In the red-eared slider turtle (Trachemys scripta), a species with temperature-dependent sex determination (TSD), the expression of the aromatase gene during gonad development is strictly limited to the female-producing temperature. The underlying mechanism remains unknown. In this study, we identified the upstream 5′-flanking region of the aromatase gene, gonad-specific promoter, and the temperature-dependent DNA methylation signatures during gonad development in the red-eared slider turtle. The 5′-flanking region of the slider aromatase exhibited sequence similarities to the aromatase genes of the American alligator, chicken, quail, and zebra finch. A putative TATA box was located 31 bp upstream of the gonad-specific transcription start site. DNA methylation at the CpG sites between the putative binding sites of the fork head domain factor (FOX) and vertebrate steroidogenic factor 1 (SF1) and adjacent TATA box in the promoter region were significantly lower in embryonic gonads at the female-producing temperature compared the male-producing temperature. A shift from male- to female-, but not from female- to male-, producing temperature changed the level of DNA methylation in gonads. Taken together these results indicate that the temperature, particularly female-producing temperature, allows demethylation at the specific CpG sites of the promoter region which leads the temperature-specific expression of aromatase during gonad development.
Highlights
Temperature-dependent sex determination (TSD) is an example of developmental plasticity where the ambient temperature of the embryos leads to the development of the bipotential gonads into either testes or ovaries
The 4113 bp of slider aromatase 59-flanking region near the ATG was pair-aligned with the aromatase gene sequence of four different species: American alligator (Alligator mississippiensis), chicken (Gallus gallus), quail (Coturnix coturnix), and zebra finch (Taeniopygia guttata)
These species were selected because of their sequence similarities in the aromatase 59-flanking region to the slider aromatase according to a nucleotide BLAST search (National center for biotechnology information, Bethesda, MD)
Summary
Temperature-dependent sex determination (TSD) is an example of developmental plasticity where the ambient temperature of the embryos leads to the development of the bipotential gonads into either testes or ovaries. In TSD species such as the American alligator and some turtle species, gonadal development can be modified by the concentration of sex steroid hormones in the surrounding system of the embryos. An excess of either testosterone or estrogen during gonadal differentiation leads to testicular or ovarian development, respectively, regardless of the surrounding temperature [1,2,3]. Blocking aromatase activity with aromatase inhibitors during gonad development results in a redirection of the putative gonadal sex usually determined by genetic- or environmental- signals in birds, reptiles, and fish [10–
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