Abstract
BackgroundLeft-right (LR) organ asymmetries are a common feature of metazoan animals. In many cases, laterality is established by a conserved asymmetric Nodal signaling cascade during embryogenesis. In most vertebrates, asymmetric nodal induction results from a cilia-driven leftward fluid flow at the left-right organizer (LRO), a ciliated epithelium present during gastrula/neurula stages. Conservation of LRO and flow beyond the vertebrates has not been reported yet.ResultsHere we study sea urchin embryos, which use nodal to establish larval LR asymmetry as well. Cilia were found in the archenteron of embryos undergoing gastrulation. Expression of foxj1 and dnah9 suggested that archenteron cilia were motile. Cilia were polarized to the posterior pole of cells, a prerequisite of directed flow. High-speed videography revealed rotating cilia in the archenteron slightly before asymmetric nodal induction. Removal of cilia through brief high salt treatments resulted in aberrant patterns of nodal expression. Our data demonstrate that cilia - like in vertebrates - are required for asymmetric nodal induction in sea urchin embryos.ConclusionsBased on these results we argue that the anterior archenteron represents a bona fide LRO and propose that cilia-based symmetry breakage is a synapomorphy of the deuterostomes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12861-016-0128-7) contains supplementary material, which is available to authorized users.
Highlights
Left-right (LR) organ asymmetries are a common feature of metazoan animals
One major question has remained unanswered: how does symmetry breakage upstream of asymmetric nodal induction occur in echinoderms? Do sea urchin embryos possess a left-right organizer (LRO) or an evolutionary functional precursor that induces asymmetric nodal expression? Do archenteron cells possess cilia and, if so, are these required to induce asymmetric nodal expression? Using descriptive and functional approaches we show that (1) archenteron cells in the sea urchin larva harbor monocilia; (2) archenteron cilia are polarized and motile; and (3) cilia are required for asymmetric nodal induction
As an entry point into studying sea urchin symmetry breakage, we investigated the presence of cilia on staged gastrula embryos by performing immunofluorescence (IF) with a well-characterized anti-acetylated α-tubulin antibody
Summary
Left-right (LR) organ asymmetries are a common feature of metazoan animals. In many cases, laterality is established by a conserved asymmetric Nodal signaling cascade during embryogenesis. The secreted transforming growth factor beta (TGFβ) Nodal binds to its receptor which results in the activation of its own transcription and that of its negative feedback inhibitor lefty (left-right determination factor), another The event activating this highly conserved developmental program is referred to as symmetry breakage. The vertebrate LRO (known as Kupffer’s vesicle in fish, gastrocoel roof plate (GRP) in amphibians, and posterior notochord or ventral node in mammals) represents a field of mono-ciliated cells at the posterior end of the forming notochord, flanked by endodermal archenteron cells [6,7,8] This unique tissue, which develops during early neurula stages, consists of superficially located mesendodermal
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