Abstract

Environmental conditions can cause phenotypic changes, part of which can be inherited by subsequent generations via soma-to-germline communication. However, the signaling molecules or pathways that mediate intertissue communication remain unclear. Here, we show that intertissue small RNA communication systems play a key role in the acquisition and inheritance of hormesis effects – stress-induced stress resistance – in Caenorhabditis elegans. The miRNA-processing enzyme DRSH-1 is involved in both the acquisition and the inheritance of hormesis, whereas worm-specific Argonaute (WAGO) proteins, which function with endo-siRNAs, are involved only in its inheritance. Further analyses demonstrate that the miRNA production system in the neuron and the small RNA transport machinery in the intestine are both essential for its acquisition and that both the transport of small RNAs in the germline and the germline Argonaute HRDE-1 complex are required for its inheritance. Our results thus demonstrate that overlapping and distinct roles of small RNA systems in the acquisition and inheritance of hormesis effects.

Highlights

  • Environmental conditions can cause phenotypic changes, part of which can be inherited by subsequent generations via soma-to-germline communication

  • As soma-to-germline communication is important for the acquisition and transmission of hormesis[5], we examined the role of small RNAs, which function in somatic tissues: endo-siRNAs and micro RNAs (miRNAs), in these processes (Fig. 1a)

  • We have shown the essential role of the intertissue small RNA communication systems in the inheritance of hormesis in C. elegans

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Summary

Introduction

Environmental conditions can cause phenotypic changes, part of which can be inherited by subsequent generations via soma-to-germline communication. We show that intertissue small RNA communication systems play a key role in the acquisition and inheritance of hormesis effects – stress-induced stress resistance – in Caenorhabditis elegans. Transmission of a heritable trait over generations requires accurate intergenerational regulation of several sets of genes responsible for the trait in descendants It remains unknown how parental generations transform environmental information into epigenetic changes in specific genes during soma-to-germline communication. We examined the role of small RNAs in the acquisition and inheritance of hormesis, that is, the osmotic stress-induced increase in resistance to oxidative stress in C. elegans. Our results reveal that intertissue communications by two distinct classes of small RNAs mediate the conversion of parental environmental conditions into epigenetic information, which could be maintained and inherited to the offspring

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