Geometric control of ciliated band regulatory states in the sea urchin embryo

Abstract

The trapezoidal ciliated band (CB) of the postgastrular sea urchin embryo surrounds the oral ectoderm, separating it from adjacent embryonic territories. Once differentiated, the CB is composed of densely arranged cells bearing long cilia that endow the larva with locomotion and feeding capability. The spatial pattern from which the CB will arise is first evidenced during pregastrular stages by expression of the pioneer gene onecut. Immediately after gastrulation, the CB consists of four separate regulatory state domains, each of which expresses a unique set of transcription factors: (1) the oral apical CB, located within the apical neurogenic field; (2) the animal lateral CB, which bilaterally separates the oral from aboral ectoderm; (3) the vegetal lateral CB, which bilaterally serves as signaling centers; and (4) the vegetal oral CB, which delineates the boundary with the underlying endoderm. Remarkably, almost all of the regulatory genes specifically expressed within these domains are downregulated by interference with SoxB1 expression, implying their common activation by this factor. Here, we show how the boundaries of the CB subdomains are established, and thus ascertain the design principle by which the geometry of this unique and complex regulatory state pattern is genomically controlled. Each of these boundaries, on either side of the CB, is defined by spatially confined transcriptional repressors, the products of regulatory genes operating across the border of each subdomain. In total this requires deployment of about ten different repressors, which we identify in this work, thus exemplifying the complexity of information required for spatial regulatory organization during embryogenesis.

Neurogenesis in sea urchin embryos and the diversity of deuterostome neurogenic mechanisms

“…The ciliary band appears to form as a consequence of being protected from Nodal and BMP signaling by the antagonists Lefty and Chordin Bradham et al, 2009;Lapraz et al, 2009;Saudemont et al, 2010;Yaguchi et al, 2010). Oral and aboral ectoderm are fields of cells with bilateral subdomains in which distinct regulatory programs appear to operate (Chen et al, 2011;Li et al, 2012;Barsi et al, 2015). Our data indicate that neurons arise within the ciliary bands and adjacent regions of oral and aboral ectoderm.…”

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

“…1H, 2 -5). This observation starkly contrasts with that in euechinoids, in which onecut is observed ubiquitously and later delimited as a whole to the CB territory by transcriptional repressors in the OE and AE (28,67). Irxa initiates zygotic expression at midblastula stage (∼14 hpf) in Et, and by 28 hpf is observed broadly in AE (Fig.…”

“…This structure has undergone frequent modification in the lineages leading to modern sea urchins (64). In euechinoids, Goosecoid (gsc), Onecut, and Irxa contribute to the geometric patterning of CB formation (28,40,65). In euechinoids, gsc is expressed in OE and is directly downstream of Nodal signaling (40), onecut (also known as hnf6) is a maternal factor in euechinoids that is later restricted to a region at the boundaries of OE and AE where progenitor CB territory forms, and irxa is expressed exclusively in AE downstream of Bmp2/4 and Tbx2/3 (40,66).…”

“…Research on the early development of the euechinoid purple sea urchin Strongylocentrotus purpuratus (Sp) has brought into high resolution the players and molecular logic directing developmental GRNs that specify Sp's early embryonic domains (19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30). Abundant comparative evidence exists for other euechinoid taxa as well, including Lytechinus variegatus (Lv) (31)(32)(33)(34)(35)(36)(37) and Paracentrotus lividus (Pl) (38)(39)(40)(41)(42).…”

Genome-wide identification of enhancer elements

“…In the sea urchin embryo, onecut [previously referred to as hnf6 (Otim et al, 2004)] encodes a pioneer factor whose zygotic expression pattern delineates a neurogenic field from which the ciliated band will arise (Barsi, Li, et al, 2015;Otim et al, 2004;Poustka et al, 2004). The ciliated band, once fully developed, is a structure that confers upon the larva the ability to both swim and feed.…”