Transgenerational epigenetics in the germline cycle of Caenorhabditis elegans

Epigenetic mechanisms create variably stable changes in gene expression through the establishment of heritable states of chromatin architecture. While many epigenetic phenomena are, by definition, heritably passed through cell division during animal and plant development, evidence suggests that ‘epigenetic states’ may also be inherited across multiple generations. Work in the nematode Caenorhabditis elegans has uncovered a number of mechanisms that participate in regulating the transgenerational passage of epigenetic states. These mechanisms include some that establish and maintain heritable epigenetic information in the form of histone modifications, as well as those that filter the epigenetic information that is stably transmitted. The information appears to influence and help guide or regulate gene activity and repression in subsequent generations. Genome surveillance mechanisms guided by small RNAs appear to be involved in identifying and directing heritable repression of genomic elements, and thus may participate in filtering information that is inappropriate for stable transmission. This review will attempt to summarize recent findings that illustrate this simple nematode to be a truly elegant resource for defining emerging biological paradigms. As the cell lineage that links generations, the germline is the carrier of both genetic and epigenetic information. Like genetic information, information in the epigenome can heritably affect gene regulation and phenotype; yet unlike genetic information, the epigenome of the germ lineage is highly modified within each generation. Despite such alterations, some epigenetic information is highly stable across generations, leading to transgenerationally stable phenotypes that are unlinked to genetic changes. Studies in the nematode C. elegans have uncovered mechanisms that contribute to transgenerational repression as well as to the expression of genes that rely on histone modifying machinery and/or non-coding RNA-based mechanisms. These studies indicate that epigenetic mechanisms operating within the germ cell cycle of this organism filter and maintain an epigenetic memory that is required for germ cell function and can also influence gene expression in somatic lineages.