Insights into transgenerational epigenetics from studies of ciliates

Abstract

Epigenetics, a term with many meanings, can be broadly defined as the study of dynamic states of the genome. Ciliates, a clade of unicellular eukaryotes, can teach us about the intersection of epigenetics and evolution due to the advantages of working with cultivable ciliate lineages, plus their tendency to express extreme phenotypes such as heritable doublet morphology. Moreover, ciliates provide a powerful model for studying epigenetics given the presence of dimorphic nuclei - a somatic macronucleus and germline micronucleus - within each cell. Here, we exemplify the power of studying ciliates to learn about epigenetic phenomena. We highlight "classical" examples from morphology and physiology including cortical inheritance, mating type determination, and serotype expression. In addition, we detail molecular studies of epigenetic phenomena, including: DNA elimination; alternative processing and unscrambling; and copy number determination. Based on the implications of these studies, we discuss epigenetics as a possible functional mechanism for rapid speciation in ciliates.

Keywords: Ciliates; Cortical inheritance; DNA processing; Mating type determination; Serotype inheritance; Transgenerational epigenetics.

Fig. 1

Simplified version of nuclear morphology following conjugation/sexual reproduction in ciliates, with the small round circles representing micronuclei: A) one haploid micronucleus is exchanged between conjugating cells; B) a zygotic nucleus is formed in the presence of the parental macronucleus; C–D) the zygotic nucleus undergoes division and daughter nuclei differentiate into a new micronucleus and macronucleus; D) the parental macronucleus degrades and is replaced by the new macronucleus.

Fig. 2

Two “classical” examples of epigenetic phenomena in ciliates. Cortical inheritance: following asexual reproduction, the wild type singlet produces progeny that are also singlets (A) while mutant doublets produce doublet offspring (B). Non-Mendelian examples of mating type determination: in karyonidal inheritance, mating type varies either stochastically or is determined by changing environmental factors (e.g. temperature, time of day; C); in cytoplasmic inheritance mating types (O and E) are maternally inherited following conjugation (D; adapted from Chalker et al., 2013; Meyer and Garnier, 2002).

Fig. 3

Two examples of molecular studies of epigenetic phenomena in ciliates. A) DNA elimination: in Oligohymenophorea, the entire micronuclear genome is transcribed into small scnRNAs. These transcripts are transported to the old macronucleus where they bind to regions of homology (MDSs indicated in light blue) and are degraded. The scnRNAs that did not bind to any region of the old macronucleus are transported into the new macronucleus and mark homologous regions (orange) for deletion. B) Alternative processing: MDSs from divergent paralogs are combined in varying orders to create gene variants. In the micronucleus (top) the MDSs labeled 1–4 are in a scrambled order. MDSs are reassembled and may be used in multiple macronuclear genes in alternative processing, which allows for the creation of several genes from two paralogs.