Old cell, new trick? Cnidocytes as a model for the evolution of novelty

Abstract

Understanding how new cell types arise is critical for understanding the evolution of organismal complexity. Questions of this nature, however, can be difficult to answer due to the challenge associated with defining the identity of a truly novel cell. Cnidarians (anemones, jellies, and their allies) provide a unique opportunity to investigate the molecular regulation and development of cell-novelty because they possess a cell that is unique to the cnidarian lineage and that also has a very well-characterized phenotype: the cnidocyte (stinging cell). Because cnidocytes are thought to differentiate from the cell lineage that also gives rise to neurons, cnidocytes can be expected to express many of the same genes expressed in their neural "sister" cells. Conversely, only cnidocytes posses a cnidocyst (the explosive organelle that gives cnidocytes their sting); therefore, those genes or gene-regulatory relationships required for the development of the cnidocyst can be expected to be expressed uniquely (or in unique combination) in cnidocytes. This system provides an important opportunity to: (1) construct the gene-regulatory network (GRN) underlying the differentiation of cnidocytes, (2) assess the relative contributions of both conserved and derived genes in the cnidocyte GRN, and (3) test hypotheses about the role of novel regulatory relationships in the generation of novel cell types. In this review, we summarize common challenges to studying the evolution of novelty, introduce the utility of cnidocyte differentiation in the model cnidarian, Nematostella vectensis, as a means of overcoming these challenges, and describe an experimental approach that leverages comparative tissue-specific transcriptomics to generate hypotheses about the GRNs underlying the acquisition of the cnidocyte identity.

Fig. 1

Anatomy of a cnidocyte. (A) Unfired. Stimulation of the cnidocil activates exocytosis of the contents of the cnidocyst. (B) Fired. The tubule is everted from the capsule of the cnidocyst.

Fig. 2

Cnidocyte development in Nematostella vectensis. (A) An adult polyp showing basic morphology. (B) DIC image of the tip of a tentacle showing the abundance of mature cnidocytes (arrows) in the tentacle’s epidermis (e). (C) Fluorescent in situ hybridization (following the protocol of Layden et al. 2012) for minicollagen 3 shows the distribution of developing cnidocytes (red) in the tentacle in this optical section; nuclei are shown in blue (DAPI). (D) EdU (following the manufacturers’ protocol; Invitrogen USA) reveals the presence of proliferative cells (green) in the tentacle’s epidermis; optical section. (E) DIC image of the ectodermal component of one mesentery showing the abundance of mature cnidocytes (arrows). (F) Confocal projection showing the presence of developing cnidocytes (red) and proliferative cells (green) in the mesentery pictured in E; nuclei as in C. (G) DIC image of an isolated nematosome with abundant mature cnidocytes (arrows). (H) Mature cnidocytes are present in aggregations (arrows) along the mesentery before the nematosomes have fully budded. (I) Fluorescent in situ hybridization for minicollagen 3 (red) overlaid on a DIC image shows developing cnidocytes in the epidermis of the body wall (e) but not in the gastrodermis or nematosome (arrow); optical section. Panel A reprinted with permission: © SERTC, South Carolina Department of Natural Resources.

Fig. 3

Venn diagram indicating target genes of interest. Targets captured in section A will include those expressed in mature cnidocytes (found in all three tissues) as well as housekeeping genes (found in all cells). Targets in section B will include the genes of the cnidocyte developmental pathway as well as genes from any other cell lineages downstream of the proliferating cells shown in Fig. 2D and F.