Multigenerational Effect of Heat Stress on the Drosophila melanogaster Sperm Proteome

J Proteome Res. 2024 May 14. doi: 10.1021/acs.jproteome.4c00205. Online ahead of print.

Abstract

The effect of the parental environment on offspring through non-DNA sequence-based mechanisms, such as DNA methylation, chromatin modifications, noncoding RNAs, and proteins, could only be established after the conception of "epigenetics". These effects are now broadly referred to as multigenerational epigenetic effects. Despite accumulating evidence of male gamete-mediated multigenerational epigenetic inheritance, little is known about the factors that underlie heat stress-induced multigenerational epigenetic inheritance via the male germline in Drosophila. In this study, we address this gap by utilizing an established heat stress paradigm in Drosophila and investigating its multigenerational effect on the sperm proteome. Our findings indicate that multigenerational heat stress during the early embryonic stage significantly influences proteins in the sperm associated with translation, chromatin organization, microtubule-based processes, and the generation of metabolites and energy. Assessment of life-history traits revealed that reproductive fitness and stress tolerance remained unaffected by multigenerational heat stress. Our study offers initial insights into the chromatin-based epigenetic mechanisms as a plausible means of transmitting heat stress memory through the male germline in Drosophila. Furthermore, it sheds light on the repercussions of early embryonic heat stress on male reproductive potential. The data sets from this study are available at the ProteomeXchange Consortium under the identifier PXD037488.

Keywords: Drosophila melanogaster; heat stress; multigenerational epigenetic inheritance; sperm proteome; white-mottled.