Small RNAs and chromatin in the multigenerational epigenetic landscape ofCaenorhabditis elegans

Abstract

For decades, it was thought that the only heritable information transmitted from one individual to another was that encoded in the DNA sequence. However, it has become increasingly clear that this is not the case and that the transmission of molecules from within the cytoplasm of the gamete also plays a significant role in heritability. The roundworm, Caenorhabditis elegans, has emerged as one of the leading model organisms in which to study the mechanisms of transgenerational epigenetic inheritance (TEI). Collaborative efforts over the past few years have revealed that RNA molecules play a critical role in transmitting transgenerational responses, but precisely how they do so is as yet uncertain. In addition, the role of histone modifications in epigenetic inheritance is increasingly apparent, and RNA and histones interact in a way that we do not yet fully understand. Furthermore, both exogenous and endogenous RNA molecules, as well as other environmental triggers, are able to induce heritable epigenetic changes that affect transcription across the genome. In most cases, these epigenetic changes last only for a handful of generations, but occasionally can be maintained much longer: perhaps indefinitely. In this review, we discuss the current understanding of the role of RNA and histones in TEI, as well as making clear the gaps in our knowledge. We also speculate on the evolutionary implications of epigenetic inheritance, particularly in the context of a short-lived, clonally propagating species. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

How does epigenetics influence the course of evolution?

“…Examples of transgenerational inheritance include responses to pathogens such as Pseudomonas [49] and possibly viruses [50,51] that are propagated over generations. These mechanisms and the overwhelming evidence for intergenerational epigenetic inheritance in C. elegans are reviewed by Frolows & Ashe [25]. They emphasize that many small RNA molecules aggregate in perinuclear granules.…”

“…It is becoming clear that perinuclear granules are intimately involved in the production of heritable small RNAs. A single generation of dysfunctional perinuclear granules leads to the creation of aberrant siRNA molecules that incorrectly silence genes for multiple generations, even after functional perinuclear granules are restored [25].…”

“…Epigenetic states are of three main kinds, which we briefly describe below. More detailed reviews of the molecular mechanisms underlying the maintenance and transmission of epigenetic states within and across generations are provided in this issue [25,26] and particularly [27].…”

Empirical evidence for epigenetic inheritance driving evolutionary adaptation

“…In animals, such as Caenorhabditis elegans (see [89]), gene expression patterns can also be transmitted even through meiosis. Transient exposure of these worms to high temperatures leads to derepression of a gene array comprising several copies of HSP90 gene.…”

Epigenetic inheritance and evolution: a historian's perspective

“…(b) Buying (more) time: the Baldwin effect Epigenetic inheritance could enhance the efficiency of the Baldwin effect in a straightforward manner, by extending the time period of the transient plastic response to new environmental challenges (see especially [65,66]). Since Baldwin [44, p. 445] and throughout the twentieth century [52, p. 12], the Baldwin effect has been primarily about 'buying time' [67], especially when environmental conditions are changing too fast for the standard mutation/selection process to adequately respond.…”