A polymorphic, thrombospondin domain-containing lectin is an oocyte marker in Hydractinia: implications for germ cell specification and sex determination

Abstract

We have identified a novel, multidomain, polymorphic lectin in the marine cnidarian Hydractinia echinata. The gene is expressed in oocytes and was therefore named CEL for cnidarian egg lectin. The predicted protein has an unusual domain architecture, consisting of variable numbers of thrombospondin type 1 domains, flanked by one N-terminal and two C-terminal galactose binding lectin domains. The diversity of the gene's transcripts results from allelic polymorphism as well as alternative splicing. Hydractinia is dioecious and its sex has been reported previously to be genetically determined. We found intersexual colonies that were functional males, but had immature CEL-positive oocytes alongside mature sperm in the same gonads. Intersexuality was observed to be common in one population but not found in others. Hermaphroditic, self-fertile colonies were found in one locality; however, in these cases gonads contained either male or female gametes without mixed ones. Intersexuality that was considered to be a very rare event is apparently a more common phenomenon, at least in some populations. True hermaphroditism also occurs in this species. CEL can be considered as a marker for early oocyte differentiation and may play a role in germ cell specification and sex determination in cnidarians.

Hydractinia, a pioneering model for stem cell biology and reprogramming somatic cells to pluripotency

“…Hence, the sexual polyps probably emit a signal instructing pluripotent cells of a defined sex to enter gametogenesis. Furthermore, gonads containing male and female gametes, simultaneously, have been reported (Mali et al, 2011).…”

“…Once the germ cell precursors have been committed, Vasa and Piwi are strongly upregulated. In oogonia a cell-type specific polymorphic thrombospondin domain-containing lectin is expressed which may fulfill functions in fertilization (Mali et al,2011).…”

Sex, polyps, and medusae: Determination and maintenance of sex in cnidarians

“…Offspring of these field-collected colonies have the same phenotype, proving that the coexistence of both gametes is a heritable trait in these animals rather than the result of a recent fusion event. In addition, since oocytes were consistently found, differences in mitotic rates cannot always explain the dominance of the male sex; perhaps a repressive signal that keeps female oocytes from maturing, similar to what is observed for Hydra, is active instead (Mali et al, 2011). Ultimately, more studies need to be conducted in different Hydractinia strains and species in order to understand the interaction of opposite-sex interstitial cell lineages in the genus.…”

“…In gonozooids, uncharacterized interstitial cells migrate from the ectoderm into the endoderm, where they are incorporated into the tissue that ultimately forms the gonophore (Weismann, ; Müller, ). This migration may be accompanied by a change from totipotent to unipotent germ cell fate (Mali et al, ). Mitotically active male germ cells are present in gonophores, suggesting that a male GSC population exists (Fig.…”

“…In this situation, the proliferative activity of male germ cells may result in a competitive advantage over female germ cells for the limited space in the forming gonophores, as oocytes appear to be displaced into the gastric cavity (Müller, ). The dominance of the male sex might be explained by different proliferation rates of the two germ‐cell populations rather than by a repressive signal (Müller, )—although this observation has been challenged by the recent collection of wild Hydractinia that make functional sperm, but also consistently harbor nonfunctional oocytes that do not reach maturity (Mali et al, ). Offspring of these field‐collected colonies have the same phenotype, proving that the coexistence of both gametes is a heritable trait in these animals rather than the result of a recent fusion event.…”