The expanding epigenetic landscape of non-model organisms

Abstract

Epigenetics studies the emergence of different phenotypes from a single genotype. Although these processes are essential to cellular differentiation and transcriptional memory, they are also widely used in all branches of the tree of life by organisms that require plastic but stable adaptation to their physical and social environment. Because of the inherent flexibility of epigenetic regulation, a variety of biological phenomena can be traced back to evolutionary adaptations of few conserved molecular pathways that converge on chromatin. For these reasons chromatin biology and epigenetic research have a rich history of chasing discoveries in a variety of model organisms, including yeast, flies, plants and humans. Many more fascinating examples of epigenetic plasticity lie outside the realm of model organisms and have so far been only sporadically investigated at a molecular level; however, recent progress on sequencing technology and genome editing tools have begun to blur the lines between model and non-model organisms, opening numerous new avenues for investigation. Here, I review examples of epigenetic phenomena in non-model organisms that have emerged as potential experimental systems, including social insects, fish and flatworms, and are becoming accessible to molecular approaches.

Keywords: Chromatin; Epigenetics; Genomics; Polyphenism.

Fig. 1.

Types of epigenetic memory. (A) Mitotic epigenetic inheritance controls the replication of epigenetic marks (yellow flag on chromosome) throughout DNA replication in S phase (middle cell) and throughout cell division in M phase (right cells). Epigenetic marks that can be inherited in this fashion include DNA methylation and, to some extent, certain histone modifications. (B) Meiotic epigenetic inheritance controls transgenerational transmission of information that does not reside in the DNA sequence. Several cases are known in plants and a handful in vertebrates such as mouse. In many cases, although the epigenetic state is visibly transmitted, the nature of the epigenetic signal in the germ cells (yellow flag, middle) remains unknown. (C) In certain cases the same epigenetic signals that transmit information throughout cell division are used to stabilize transcriptional patterns in terminally differentiated, non-dividing cells. Although the inheritance-based definition of epigenetics would exclude such mechanisms, because of the shared molecular features they are nonetheless of interest to epigenetic research.

Fig. 2.

Molecular encoding of epigenetic information. Chromatin is composed of DNA (red line) packaged around histone octamers (blue discs) into nucleosomes. (A) In addition to the DNA sequence, biological information can be encoded by chemical changes to the DNA, such as methylation (me) or histone PTMs (yellow flags). (B) Higher-order chromatin structures might also be vehicles of epigenetic information. In this case loose (left) versus dense, compact (right) chromatin correspond to active and repressed chromatin, respectively.

Fig. 3.

Examples of epigenetic plasticity in development. (A) In Daphnia, alternative phenotypes can emerge as a consequence of exposure to predator-derived chemicals (kairomones). In this case, genetically identical F1 (products of parthenogenesis) present differences in the form of a defensive structure called a ‘helmet’. The presence of the helmet can persist in later generations despite the absence of the originating stimulus. (B) In the half-smooth tongue sole Cynoglossus semilaevis, sex is genetically determined by the presence of two Z chromosomes (male) or one Z and one W chromosome (female). However, higher temperatures during the juvenile phase induce conversion of ZW females to ‘pseudomales’. Interestingly, the ZW progeny of these pseudomales will develop into more pseudomales even if the temperature remains low, suggesting an epigenetic transmission of the sex conversion.

Fig. 4.

Extreme epigenetics. (A) Eusocial insects, such as ants, encode different developmental destinies in the same genome. In most species embryos (left) and larvae (middle) are genetically indistinguishable, but they give rise to entirely different adults (right); specifically, reproductives (queens) and non-reproductives (workers). These differ not only in size and morphology, but also in physiology and behavior. (B) Adult planarians can regenerate all body tissues and structures after amputation (1). Pluripotent adult stem cells known as neoblasts (red dots) migrate to the wound site (2), create a regenerating structure called blastema (3), which eventually restores all organs of the adult animal, including the nervous system (4).