C. elegans aversive olfactory learning generates diverse intergenerational effects

J Neurogenet. 2020 Sep-Dec;34(3-4):378-388. doi: 10.1080/01677063.2020.1819265. Epub 2020 Sep 17.

Abstract

Parental experience can modulate the behavior of their progeny. While the molecular mechanisms underlying parental effects or inheritance of behavioral traits have been studied under several environmental conditions, it remains largely unexplored how the nature of parental experience affects the information transferred to the next generation. To address this question, we used C. elegans, a nematode that feeds on bacteria in its habitat. Some of these bacteria are pathogenic and the worm learns to avoid them after a brief exposure. We found, unexpectedly, that a short parental experience increased the preference for the pathogen in the progeny. Furthermore, increasing the duration of parental exposure switched the response of the progeny from attraction to avoidance. To characterize the underlying molecular mechanisms, we found that the RNA-dependent RNA Polymerase (RdRP) RRF-3, required for the biogenesis of 26 G endo-siRNAs, regulated both types of intergenerational effects. Together, we show that different parental experiences with the same environmental stimulus generate different effects on the behavior of the progeny through small RNA-mediated regulation of gene expression.

Keywords: C. elegans; Intergeneration; epigenetics; learning; olfaction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Avoidance Learning / physiology*
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Choice Behavior / physiology
  • Embryo, Nonmammalian / physiology
  • Environmental Exposure
  • Escherichia coli
  • Feeding Behavior / physiology*
  • Gene Expression Regulation / physiology*
  • Hermaphroditic Organisms
  • Mutation
  • Odorants
  • Pseudomonas aeruginosa / pathogenicity
  • RNA Interference
  • RNA, Helminth / genetics
  • RNA, Small Interfering / genetics
  • RNA-Dependent RNA Polymerase / genetics
  • RNA-Dependent RNA Polymerase / physiology*
  • Smell / physiology*

Substances

  • RNA, Helminth
  • RNA, Small Interfering
  • RNA-Dependent RNA Polymerase
  • RNA-directed RNA polymerase RRF-3, C elegans