PaxA, but not PaxC, is required for cnidocyte development in the sea anemone Nematostella vectensis

Abstract

Background Pax genes are a family of conserved transcription factors that regulate many aspects of developmental morphogenesis, notably the development of ectodermal sensory structures including eyes. Nematostella vectensis, the starlet sea anemone, has numerous Pax orthologs, many of which are expressed early during embryogenesis. The function of Pax genes in this eyeless cnidarian is unknown.ResultsHere, we show that PaxA, but not PaxC, plays a critical role in the development of cnidocytes in N. vectensis. Knockdown of PaxA results in a loss of developing cnidocytes and downregulation of numerous cnidocyte-specific genes, including a variant of the transcription factor Mef2. We also demonstrate that the co-expression of Mef2 in a subset of the PaxA-expressing cells is associated with the development with a second lineage of cnidocytes and show that knockdown of the neural progenitor gene SoxB2 results in downregulation of expression of PaxA, Mef2, and several cnidocyte-specific genes. Because PaxA is not co-expressed with SoxB2 at any time during cnidocyte development, we propose a simple model for cnidogenesis whereby a SoxB2-expressing progenitor cell population undergoes division to give rise to PaxA-expressing cnidocytes, some of which also express Mef2.DiscussionThe role of PaxA in cnidocyte development among hydrozoans has not been studied, but the conserved role of SoxB2 in regulating the fate of a progenitor cell that gives rise to neurons and cnidocytes in Nematostella and Hydractinia echinata suggests that this SoxB2/PaxA pathway may well be conserved across cnidarians.

Stem cell differentiation trajectories inHydraresolved at single-cell resolution

“…Our results therefore strongly suggest that Pax-A functions during early nematogenesis. This is concordant with a recent finding that Pax-A is required for nematogenesis during Nematostella development (65,68). Similarly, we also found evidence that suggests that an RX homeobox transcription factor (t22218) functions in basal disk development and an RFX transcription factor (t5694) functions in gland cell specification; the latter was also reported for Nematostella (Fig.…”

NvPOU4/Brain3functions as a terminal selector gene in the nervous system of the cnidarianNematostella vectensis

“…Using whole mount in situ hybridization, we first observed expression of NvPOU4 in few cells at early blastula (12 hours post fertilization at 21°C; Figure 1A). This expression occurs after the start of NvSoxB(2) expression (a gene expressed in neural progenitor cells, (Magie et al, 2005;Richards and Rentzsch, 2014)), but before expression of NvNCol3 commences (a gene expressed in differentiating cnidocytes and encoding the minicollagen structural protein of the cnidocyst capsule wall (Babonis and Martindale, 2017;Zenkert et al, 2011)). NvPOU4 is expressed in scattered cells all over the ectoderm of the embryo at gastrula stage and in scattered single cells in both ectoderm and endoderm at mid-planula stage ( Figure 1B-C).…”

“…To better characterize the cnidocyte phenotype, we performed stainings to distinguish developing from mature cnidocytes. An antibody against NvNCol3 detects the cnidocysts throughout their development, but does not detect the fully mature cnidocyst capsules (with very few exceptions) (Babonis and Martindale, 2017;Zenkert et al, 2011). The matrix of the mature cnidocysts is specifically labelled by incubation with a high concentration of 4′,6-diamidino-2-phenylindole (DAPI) in the presence of EDTA (Szczepanek et al, 2002).…”

“…anti-NCol3 (Zenker et al2011); mature cnidocytes were labelled with DAPI/EDTA as described in (Babonis and Martindale, 2017;Szczepanek et al, 2002).…”

Signaling via GABAB receptors regulates early development and neurogenesis in the basal metazoan Nematostella vectensis

“…7a). Expression of mini-collagen 3 (NvMc3), a structural protein in the stinging capsule, is extremely reduced in baclofen-treated planulae, as was expression of NvPaxA, a member of the homeodomain transcription factors family that is required for cnidocyte development (47).…”