Multi-omics analysis reveals that natural hibernation is crucial for oocyte maturation in the female Chinese alligator

Abstract

Background Hibernation in an appropriate environment not only is important for the survival of hibernators in winter, but also is crucial for breeding in the following season for many hibernating species. However, the genetic and epigenetic mechanism underlying this process remain unclear. In the current study, we performed an integrative multi-omics analysis of gonads collected from Chinese alligators that overwintered in wild cave and artificial warmroom to explore transcriptomic and epigenomic alternations in these organs. Results The data revealed that in the breeding season, female alligators were more strongly affected in terms of gene expression than males by non-hibernation because of overwintering in a warm room, especially for genes related to oocyte maturation, and this effect commenced in winter with the downregulation of STAR, which is the rate limiting factor of steroid biosynthesis. Further, miRNAs were found to play essential roles in this negative effect of overwintering in the warm room on hibernation. The upregulated miRNAs likely were responsible for the suppression of oocyte maturation in the breeding season. Finally, DNA methylome changes, especially hypomethylation, were found to play an important role in the alterations in ovarian function-related gene expression induced by non-hibernation. Conclusions Our study revealed the crucial role of hibernation quality for oocyte maturation in the Chinese alligator and the underlying genetic and epigenetic mechanisms, and highlights the importance of habitat, and especially, the overwintering site, in the conservation of not only the Chinese alligator, but also other endangered hibernators.

Genome-Wide DNA Methylation and Transcriptome Analyses Reveal Epigenetic and Genetic Mechanisms Underlying Sex Maintenance of Adult Chinese Alligator

“…We identified the sex-biased DEGs separately in summer- and winter-collected samples, rather than treating these as biological replicates, as the physiological status of the alligators differs substantially in these two seasons ( Lin et al, 2020a ). In particular, given that the biosynthesis pathways of anti-Müllerian hormone, melatonin, and steroid hormones are suppressed in the testes during winter ( Lin et al, 2020b ), we focused on the summer-collected samples in the following analysis, as these provided a more representative indication of physiological status. However, we will refer to the winter-collected data in certain instances.…”

Sex-Biased miRNAs in the Gonads of Adult Chinese Alligator (Alligator sinensis) and Their Potential Roles in Sex Maintenance

“…In the ovaries of adult Chinese alligators, the high expression of miR-148a indicates the health of the ovaries. In addition, only let-7c of the let-7 family maintained its female-biased expression in both seasons, while other family members (Let-7a, 7e, and 7f) showed female-biased expression only in summer, which may be related to the hibernation habit of Chinese alligator ( Lin et al, 2020 ).…”

“…Therefore, the Chinese alligator is a suitable biological model to study temperature-dependent sex determination, differentiation, and maintenance. Our previous studies on the gonads of the Chinese alligator have mainly focused on the process of sex differentiation in the embryonic stage ( Lin et al, 2018 ), the importance of hibernation to ovarian development ( Lin et al, 2020 ), and the genetic and epigenetic mechanisms of sex maintenance ( Lin et al, 2021 ). The default sex of the Chinese alligator embryo is female and the male determination is triggered by high temperature through calcium signals in the middle of the TSP, while miRNA also participates in the regulation of this process ( Lin et al, 2018 ).…”

Beyond the Egg and the Sperm?: How Science Has Revised a Romance through Reproductomics

“…For example, a group of researchers from Hangzhou, China, studied a critically endangered species, the Chinese alligator, in particular the female alligator’s “seasonal transcriptome” and “DNA methylome” (the set of methylation modifications in an organism’s genome) in order to investigate how the duration of hibernation and temperature of the hibernation environment influences the ability of oocytes to mature. The research team argues that “hibernation is crucial for oocyte maturation in the female Chinese alligator” (Lin et al 2020: 1). Intriguingly, such findings were not true of Chinese alligator sperm, which remained at similar quality no matter the temperature.…”

“…Intriguingly, such findings were not true of Chinese alligator sperm, which remained at similar quality no matter the temperature. This led authors to suggest: “the female alligator is more sensitive to the hibernation environment” (Lin et al 2020: 9).…”