Notch and Nodal control forkhead factor expression in the specification of multipotent progenitors in sea urchin

Abstract

SUMMARYIndirect development, in which embryogenesis gives rise to a larval form, requires that some cells retain developmental potency until they contribute to the different tissues in the adult, including the germ line, in a later, post-embryonic phase. In sea urchins, the coelomic pouches are the major contributor to the adult, but how coelomic pouch cells (CPCs) are specified during embryogenesis is unknown. Here we identify the key signaling inputs into the CPC specification network and show that the forkhead factor foxY is the first transcription factor specifically expressed in CPC progenitors. Through dissection of its cis-regulatory apparatus we determine that the foxY expression pattern is the result of two signaling inputs: first, Delta/Notch signaling activates foxY in CPC progenitors; second, Nodal signaling restricts its expression to the left side, where the adult rudiment will form, through direct repression by the Nodal target pitx2. A third signal, Hedgehog, is required for coelomic pouch morphogenesis and institution of laterality, but does not directly affect foxY transcription. Knockdown of foxY results in a failure to form coelomic pouches and disrupts the expression of virtually all transcription factors known to be expressed in this cell type. Our experiments place foxY at the top of the regulatory hierarchy underlying the specification of a cell type that maintains developmental potency.

Essential elements for translation: the germline factor Vasa functions broadly in somatic cells

“…Voronina et al, 2008;Juliano and Wessel, 2009; and data not shown). At present, it is unknown what regulates Vasa expression in these late larvae, but recent work (Materna et al, 2013) suggests that the transcription factor FoxY controls the multipotency of coelomic pouch cells, and that, in turn, FoxY is activated by Delta/Notch signalling, beginning in the 16-cell stage.…”

Contribution of hedgehog signaling to the establishment of left–right asymmetry in the sea urchin

“…Establishing left-right asymmetry therefore presents a crucial step in the development of the sea urchin. Several studies have examined the mechanisms behind left-right asymmetry in the sea urchin and have identified a conserved cohort of molecules including Nodal, BMP, Delta and Hedgehog providing a unique insight into the evolution of left-right axis determination (Bessodes et al, 2012; Duboc et al, 2005; Luo and Su, 2012; Walton et al, 2009; Materna et al, 2013; Su, 2014). …”

The characterization of larval homology: transcriptomic insights into the origin and evolution of animal life cycles

“…All orthologous and/or paralogous TFs in Amphimedon, Acropora, Haliotis, Balanoglossus, Strongylocentrotus, and Herdmania were identified based on the shared Homology Groups (HG) with known TFs from humans (Vaquerizas et al 2009), Strongylocentrotus (Dobias et al 1996, Kontrogianni-Konstantopoulos et al 1996, Materna et al 2013, Burke et al 2006, Fernandez-Guerra et al 2006, Sodergren et al 2006, McCauley et al 2010, Sharma and Ettensohn 2010, Peter and Davidson 2011, Tu et al 2012, Yazaki et al 2014, Varrella et al 2016,…”

“…In Haliotis, I recovered many genes containing chitin-related protein domains, which is a known component of molluscan shells (Peters 1972, Jackson et al 2010a, and may also play important enzymatic or signaling functions in other molluscs (Schönitzer and Weiss 2007). In Strongylocentrotus, I found an overrepresentation of DEGs containing the DSL (Delta serrate ligand; PF01414) domain, along with EGF (PF00008) and ANK (Ankyrin repeat; PF13606) domains that together make up essential components of the Notch signaling receptors (Gazave et al 2009, Kopan andIlagan 2009), which has a well-established role in sea urchin endomesoderm gene regulatory networks (GRNs; Sweet et al 1999, Materna et al 2013. Additionally I found an enrichment of the asparagine synthase domain (PF00733), which is presumably responsible for making asparagine -an essential component of sea urchin skeleton (Farach-Carson et al 1989).…”

“…For instance, I identified differentially expressed orthologs of Cbfb in all species except Herdmania , Tu et al 2012, which has been implicated in cell differentiation and expressed in the mid-and hind-gut of the sea urchin larvae , and orthologs of the e2f3 TF in all species except Acropora (Burke et al 2006, Fernandez-Guerra et al 2006, Tu et al 2012, Materna et al 2013, which has been implicated in neural system development due to an expression in apical ectodermal tissue in the sea urchin (Burke et al 2006). Additionally, I identified six TFs that are differentially expressed in four different species, some of which imply eumetazoan-specific (such as orthologs of TCF/Par), bilaterian-specific (such as Thr), or metazoan-specific conservation (such as Six1/2, Klf, Ezh, and Arx) , Otim et al 2004, Burke et al 2006, Peter and Davidson 2011, Tu et al 2012, Cui et al 2014, Krupke and Burke 2014, Barsi and Davidson 2016, which I identified as differentially expressed in all sampled deuterostome taxa, and is known to be important for larval ciliary bands in Strongylocentrotus (Barsi et al 2015, Barsi andDavidson 2016).…”