Abstract
BackgroundPax 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.
Highlights
Paired box (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
We show that PaxA is expressed exclusively in developing cnidocytes, that knockdown of PaxA results in decreased expression of many cnidocyte-specific genes, and that co-expression of Mef2 splice variant IV (Mef2IV) in a subset of the PaxA-expressing cells defines a second lineage of developing cnidocyte
Cnidogenesis occurs continuously throughout the ectoderm in N. vectensis To study the differentiation of cnidocytes in situ, we used a combination of markers that label distinct stages of cnidocyst development (Fig. 2)
Summary
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. The proteins that comprise the structural elements of the cnidocyst (tubule, harpoon, and capsule wall) are largely cnidocyte specific and include the minicollagens and nematogalectins [5,6,7,8]. Initial synthesis of the structures comprising the cnidocyst is followed by invagination of the eversible tubule and swelling of the capsule to generate the high intracapsular osmotic pressure that enables rapid discharge of the mature organelle [11]. This final step of cnidocyst maturation requires the synthesis of poly-γ-glutamate by enzymes found within the developing capsule [12,13,14]. Further surveys of gene and protein expression in cnidocytes from across cnidarians have revealed that these novel cells are highly heterogeneous, expressing both novel (cnidarian-specific) and conserved genes [7, 9, 15, 17,18,19,20]
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