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.