Pax37 gene function in Oikopleura dioica supports a neuroepithelial-like origin for its house-making Fol territory

Larvacean tunicates feature a spectacular innovation not seen in other animals - the trunk oikoplastic epithelium (OE). This epithelium produces a house, a large and complex extracellular structure used for filtering and concentrating food particles. Previously we identified several homeobox transcription factors expressed during early OE patterning. Among these are two Pax3/7 duplicates that we named Pax37A and Pax37B. The vertebrate homologs, PAX3 and PAX7 are involved in developmental processes related to neural crest and muscles. In the ascidian tunicate Ciona intestinalis, Pax3/7 is playing a role in the development of cells deriving from the neural plate border, including trunk epidermal sensory neurons and tail nerve cord neurons, as well as in the neural tube closure. Here we have investigated the roles of Oikopleura dioica Pax37A and Pax37B in the development of the OE, using CRISPR-Cas9 mutant lines and analyzing scRNA-seq data from wild-type animals that we compared with scRNA-seq data from C. intestinalis. We revealed that Pax37B but not Pax37A is essential for the differentiation of cell fields that produce the food concentrating filter of the house: the anterior Fol, giant Fol and Nasse cells. Trajectory analysis supports that these cells have a neuroepithelial-like transcriptional signature. We propose that the highly specialized secretory epithelial cells of the Fol region either maintained or evolved neuroepithelial features such as “glue” secreting collocytes of ascidians. Their development seems to be controlled by a fragmented GRN that also operates in ascidian epidermal neurons. Overall design: To reveal downstream genes that are regulated by Pax37b, we compared the transcriptomes of Pax37b-/- individuals to wild-type transcriptomes