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Multigenerational effect of heat stress on the Drosophila melanogaster sperm proteome

ABSTRACT: The notion that genes are the sole units of heredity and that a barrier exists between soma and germline has been a major hurdle in elucidating the heritability of traits that were observed to follow a non-Mendelian inheritance pattern. It was only after the conception of “epigenetics” by C. H. Waddington that the effect of parental environment on subsequent generations via non-DNA sequence-based mechanisms, such as DNA methylation, chromatin modifications, non-coding RNAs and proteins, could be established in various organisms, now referred to as multigenerational epigenetic inheritance. Despite the growing body of evidence, the male gamete-derived epigenetic factors that mediate the transmission of such phenotypes are seldom explored, particularly in the model organism Drosophila melanogaster. Using the heat stress-induced multigenerational epigenetic inheritance paradigm in a widely used position-effect variegation line of Drosophila, named white-mottled, we have dissected the effect of heat stress on the sperm proteome in the current study. We demonstrate that multiple successive generations of heat stress at the early embryonic stage results in a significant downregulation of proteins associated with translation, chromatin organization, microtubule-based processes, and generation of metabolites and energy in the Drosophila sperms. Based on our findings, we propose chromatin-based epigenetic mechanisms, a well-established mechanism for environmentally induced multigenerational effects, as a plausible way of transmitting heat stress memory via the male germ line in subsequent generations. Moreover, we demonstrate the effect of multiple generations of heat stress on the reproductive fitness of Drosophila, shedding light on the adaptive or maladaptive potential of heat stress-induced multigenerational phenotypes.

INSTRUMENT(S): Q Exactive HF

ORGANISM(S): Drosophila Melanogaster (fruit Fly)

TISSUE(S): Spermatozoon, Sperm

DISEASE(S): Disease Free

SUBMITTER: Shagufta Khan

LAB HEAD: Rakesh Kumar Mishra

PROVIDER: PXD037488 | Pride | 2024-05-10

REPOSITORIES: Pride

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			Action	DRS
	ESC-HF-S1-N4-1A-90min-301020-Shagufta.raw	Raw
	ESC-HF-S1-W-1NI-A-200420-Shagufta.raw	Raw
	ESC-HF-S10-N4-3B-90min-301020-Shagufta.raw	Raw
	ESC-HF-S10-W-3NI-B-200420-Shagufta.raw	Raw
	ESC-HF-S11-N4-3C-90min-301020-Shagufta.raw	Raw

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Project description:Environmental stress-induced transgenerational epigenetic effects have been observed in various model organisms and human. The capacity and mechanism of such phenomena, particularly in animals, are poorly understood. In C. elegans, siRNA mediates transgenerational gene silencing through the germline nuclear RNAi pathway. At the organismal level, this pathway plays a transgenerational role in maintaining the germline immortality when C. elegans is under a mild heat stress. However, the underlying molecular mechanism is unknown. In this study, we performed a 12-generation temperature-shift experiment (15˚C->23˚C->15˚C) using the wild type (N2) and a mutant strain that lacks the germline-specific nuclear AGO protein HRDE-1/WAGO-9. We found that the temperature-sensitive mortal germline (Mrt) phenotype of the hrde-1 mutant is reversible, indicating a transgenerational cumulative but also reversible nature of the underlying molecular cause. By taking the whole-genome RNA and chromatin profiling approaches, we revealed an epigenetic role of HRDE-1 in repressing heat stress-induced transcriptional activation of over 280 genes, predominantly in or near LTR retrotransposons. Strikingly, for some of these elements, the heat stress-induced transcription becomes progressively activated in the hrde-1 mutant over several generations under heat stress. Furthermore, the effect of heat stress-induced transcription activation is heritable for at least two generations after the heat stress. Interestingly, the siRNA expression of these genes tend to be heat-inducible in the wild type animals, but not in the hrde-1 mutant, suggesting a role of siRNAs in repressing heat-inducible elements. Our study revealed a novel phenomenon of transgenerational feed-forward transcriptional activation, which is normally repressed in the wild type C. elegans by the germline nuclear RNAi pathway. It also provides a new paradigm to study epigenetic circuitry that connects the environment and gene regulation in the germline.

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Multigenerational effect of heat stress on the Drosophila melanogaster sperm proteome

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