Distinct transcriptional responses to mild cold versus warm temperatures in adult Drosophila melanogaster ovaries
Temperature influences fertility across diverse organisms, yet the mechanisms underlying how suboptimal temperatures affect gamete production and quality remain largely unknown. We previously showed that chronic exposure of adult Drosophila melanogaster females to mild cold promotes the maintenance of germline stem cells (GSCs) and high oocyte quality over time despite reducing the rates of…
Temperature profoundly impacts fertility in various organisms, but the precise mechanisms by which suboptimal temperatures alter gamete production and quality remain poorly understood. Our prior research demonstrated that exposing adult female Drosophila melanogaster to mild cold induces the preservation of germline stem cells (GSCs) and superior oocyte quality over time, while warm temperatures result in early germline cyst and vitellogenic follicle death, accompanied by a marked reduction in oocyte quality.
To shed light on the underlying molecular mechanisms responsible for these distinct responses, we compared the ovarian transcriptomes of flies maintained at 18°C or 29°C to those of 25°C controls. Our findings revealed that the ovary undergoes a slew of gene upregulation or downregulation in response to mild cold and warm temperatures, contrasting with passive thermodynamic changes.
Enrichment analysis of gene sets indicated that 18°C activates neuronal signaling pathways, while 29°C dampens them. However, the majority of genes exhibit temperature-specific regulation patterns: 29°C triggers the upregulation of synaptic transmission genes and the downregulation of lipid biosynthesis genes, while 18°C promotes actin cytoskeleton genes and suppresses cell adhesion and lipid organization genes.
Interestingly, mild cold or warm temperature selectively modulates (either up or down) the expression of unique sets of transposable elements (TEs), suggesting the existence of temperature-dependent TE regulatory mechanisms and/or downstream effects. Finally, we observed that GSCs exposed to 18°C display elevated retrotransposon R2 transcript levels, larger nucleolar size, and heightened levels of the known stemness factor phosphorylated Mad, pointing towards a model wherein increased ribosome biogenesis supports enhanced stemness signaling to maintain GSCs during mild cold exposure.
Our results elucidate possible molecular mechanisms and raise intriguing questions for future investigations into how temperature modulates gene expression and ultimately influences germline development and quality, which are crucial for species survival.
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