Heritable Transmission of Stress Resistance by High Dietary Glucose in Caenorhabditis elegans

Abstract

Glucose is a major energy source and is a key regulator of metabolism but excessive dietary glucose is linked to several disorders including type 2 diabetes, obesity and cardiac dysfunction. Dietary intake greatly influences organismal survival but whether the effects of nutritional status are transmitted to the offspring is an unresolved question. Here we show that exposing Caenorhabditis elegans to high glucose concentrations in the parental generation leads to opposing negative effects on fecundity, while having protective effects against cellular stress in the descendent progeny. The transgenerational inheritance of glucose-mediated phenotypes is dependent on the insulin/IGF-like signalling pathway and components of the histone H3 lysine 4 trimethylase complex are essential for transmission of inherited phenotypes. Thus dietary over-consumption phenotypes are heritable with profound effects on the health and survival of descendants.

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

“…7 for an overview model). Our findings are in agreement with the previous work of Tauffenberger and Parker15, in which they demonstrated that high dietary glucose in the P0 generation induces hormesis effects in the unstressed next generation, and that H3K4me3 modifiers and the insulin/IGF-like signalling components are involved in the underlying mechanisms. Our study newly revealed that exposure of P0 parents to various stressors induces similar hormesis effects in the subsequent generations, indicating the generality of the transgenerational inheritance of acquired traits.…”

“…Non-lethal exposure to stressors in early life can increase the stress resistance of animals and extend the lifespan, suggesting the long-lasting hormesis effects throughout life101112. Recent studies suggest that ancestral environmental conditions can influence the phenotypes of progeny13141516. However, it is unclear whether beneficial hormesis effects can be transmitted to the offspring.…”

Transgenerational Effects of Early Life Starvation on Growth, Reproduction, and Stress Resistance inCaenorhabditis elegans

“…Either way, inheritance of increased starvation survival and thermotolerance is consistent with an adaptive response to extended starvation despite reduced growth and fertility. High glucose consumption also decreases fertility but increases resistance to oxidative stress in progeny (Tauffenberger and Parker 2014), and this combination of effects could theoretically increase fitness in adverse conditions (Ratcliff et al 2009). Although we argue against a thrifty phenotype in the animals exposed to extended starvation, inheritance of increased resistance to starvation and heat suggests a conceptually related example of the animal using experience to anticipate future conditions.…”

Epigenetic regulation of ageing: linking environmental inputs to genomic stability

“…In C. elegans , exposure of the parental generation to high glucose promotes resistance to oxidative stress and can reduce neurodegeneration in the F1 progeny 169 . The transmission of stress-resistance requires intact sir-2.1 and genes encoding COMPASS H3K4 methyltransferase complex components WDR-5 and SET-2, although changes in global H3K4me3 levels are not inherited along with stress resistance 169 . In flies, exposure to heat shock or osmotic stress induces heterochromatin changes that persist over several generations in the absence of stress 11 .…”