Environmental stresses induce transgenerationally inheritable survival advantages via germline-to-soma communication in Caenorhabditis elegans

Saya Kishimoto,Emiko Okabe,Eisuke Nishida,Masanori Nono,Masaharu Uno

doi:10.1038/ncomms14031

Abstract

Hormesis is a biological phenomenon, whereby exposure to low levels of toxic agents or conditions increases organismal viability. It thus represents a beneficial aspect of adaptive responses to harmful environmental stimuli. Here we show that hormesis effects induced in the parental generation can be passed on to the descendants in Caenorhabditis elegans. Animals subjected to various stressors during developmental stages exhibit increased resistance to oxidative stress and proteotoxicity. The increased resistance is transmitted to the subsequent generations grown under unstressed conditions through epigenetic alterations. Our analysis reveal that the insulin/insulin-like growth factor (IGF) signalling effector DAF-16/FOXO and the heat-shock factor HSF-1 in the parental somatic cells mediate the formation of epigenetic memory, which is maintained through the histone H3 lysine 4 trimethylase complex in the germline across generations. The elicitation of memory requires the transcription factor SKN-1/Nrf in somatic tissues. We propose that germ-to-soma communication across generations is an essential framework for the transgenerational inheritance of acquired traits, which provides the offspring with survival advantages to deal with environmental perturbation.

Highlights

Hormesis is a biological phenomenon, whereby exposure to low levels of toxic agents or conditions increases organismal viability
Our analysis reveal that the insulin/insulin-like growth factor (IGF) signalling effector DAF-16/FOXO and the heat-shock factor Heatshock factor-1 (HSF-1) in the parental somatic cells mediate the formation of epigenetic memory, which is maintained through the histone H3 lysine 4 trimethylase complex in the germline across generations
Our findings are in agreement with the previous work of Tauffenberger and Parker[15], in which they demonstrated that high dietary glucose in the P0 generation induces hormesis effects in the unstressed generation, and that H3K4me[3] modifiers and the insulin/IGF-like signalling components are involved in the underlying mechanisms

Summary

Introduction

Hormesis is a biological phenomenon, whereby exposure to low levels of toxic agents or conditions increases organismal viability It represents a beneficial aspect of adaptive responses to harmful environmental stimuli. Adaptive responses to low-doses storessors, have been reported to improve the functional ability of cells and organisms across a variety of animal species[6,7,8,9] Such defensive mechanisms against environmental deterioration are crucial to the survival of species in the wild. Recent studies suggest that ancestral environmental conditions can influence the phenotypes of progeny[13,14,15,16] It is unclear whether beneficial hormesis effects can be transmitted to the offspring

Methods

Results

Conclusion