Abstract

In recent years, studies in Caenorhabditis elegans nematodes have shown that different stresses can generate multigenerational changes. Here, we show that worms that grow in liquid media, and also their plate-grown progeny, are different from worms whose ancestors were grown on plates. It has been suggested that C. elegans might encounter liquid environments in nature, although actual observations in the wild are few and far between. By contrast, in the laboratory, growing worms in liquid is commonplace, and often used as an alternative to growing worms on agar plates, to control the composition of the worms' diet, to starve (and synchronize) worms or to grow large populations for biochemical assays. We found that plate-grown descendants of M9 liquid medium-grown worms were longer than control worms, and the heritable effects were already apparent very early in development. We tested for the involvement of different known epigenetic inheritance mechanisms, but could not find a single mutant in which these inter-generational effects are cancelled. While we found that growing in liquid always leads to inter-generational changes in the worms' size, trans-generational effects were found to be variable, and in some cases, the effects were gone after one to two generations. These results demonstrate that standard cultivation conditions in early life can dramatically change the worms' physiology in adulthood, and can also affect the next generations. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Highlights

  • You could not step twice into the same river (Heraclitus)In comparison with Mendelian inheritance, which entails faithful transmission of discrete packets of information which do not blend or dilute [1], heritable epigenetic data are ‘soft’, or ‘fluid’, as they change as a function of time, and in response to physiological processes [2].Generally, mechanisms that allow trans-generational epigenetic effects, namely transmission of information to progeny not exposed to the original trigger, are still poorly understood [3]

  • In the course of conducting many experiments with liquid-grown worms, we noticed that after growth in liquid medium, the worms exhibit a different morphology in comparison with plate-grown worms

  • We show that growth in liquid medium under laboratory conditions changes the morphology of C. elegans worms and the morphology of their progeny

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Summary

Introduction

You could not step twice into the same river (Heraclitus)In comparison with Mendelian inheritance, which entails faithful transmission of discrete packets of information which do not blend or dilute [1], heritable epigenetic data are ‘soft’, or ‘fluid’, as they change as a function of time, and in response to physiological processes [2].Generally, mechanisms that allow trans-generational epigenetic effects, namely transmission of information to progeny not exposed to the original trigger, are still poorly understood [3]. Many studies with C. elegans have demonstrated that different environmental challenges leave a trace in the progeny, for example, viral infections [5,6,7], starvation [8,9,10,11], high temperatures [12,13,14], high osmolality [15,16] and exposure to toxins [15]. Such stressors can lead to short- or long-term gene expression alterations and physiological changes. The inheritance of some of these responses is associated with changes in heritable small RNAs [8,13,14] and/or is correlated with alteration in histone modifications (for example, of H3K4me [15,17])

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