Distinct regulatory states control the elongation of individual skeletal rods in the sea urchin embryo

Abstract

Background: Understanding how gene regulatory networks (GRNs) control developmental progression is a key to the mechanistic understanding of morphogenesis. The sea urchin larval skeletogenesis provides an excellent platform to tackle this question. In the early stages of sea urchin skeletogenesis, skeletogenic genes are uniformly expressed in the skeletogenic lineage. Yet, during skeletal elongation, skeletogenic genes are expressed in distinct spatial sub-domains. The regulation of differential gene expression during late skeletogenesis is not well understood.Results: Here we reveal the dynamic expression of the skeletogenic regulatory genes that define a specific regulatory state for each pair of skeletal rods, in the sea urchin Paracentrotus lividus. The vascular endothelial growth factor (VEGF) signaling, essential for skeleton formation, specifically controls the migration of cells that form the postoral and distal anterolateral skeletogenic rods. VEGF signaling also controls the expression of regulatory genes in cells

ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis

“…Microinjections were conducted similarly to [44]. The eggs were injected with an injection solution containing 0.12M KCl, 0.5µg/µl Rhodamine Dextran and 900µM of MASOs.…”

“…QPCR was carried out as described in [44]. Complete list of primer sequences used for the experiments in provided there.…”

“…The GRN that controls sea urchin skeletogenesis is known in great detail and shows remarkable similarity to the GRN that controls vertebrates' vascularization, suggesting a common evolutionary origin of these two tubulogenesis programs [6,36,41,42]. As the spicules elongate, the expression of key regulatory and biomineralization related genes becomes restricted to the skeletogenic cells proximal to the growing tips, possibly to promote mineral deposition at these sites [43][44][45]. Localized gene expression is regulated by signaling cues such as the Vascular Endothelial Growth Factor (VEGF) signaling [43,44].…”

Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ

“…tunicates and vertebrates) (Figure 1 A). Echinoderms, which include sea urchins and sea stars, are part of the sister group to chordates and as such occupy a critical phylogenetic position to understand evolution of vertebrate organs, while offering a series of experimental advantages (Annunziata et al, 2019; Annunziata et al, 2013; Annunziata et al, 2014; Arnone et al, 2016; Ben-Tabou de-Leon, 2022; Cary et al, 2019; Cary & Hinman, 2017; Cheatle Jarvela & Hinman, 2014; Hinman & Cheatle Jarvela, 2014; Meyer & Hinman, 2022; Morgulis et al, 2019; Morgulis et al, 2021; Tarsis et al, 2022; Wolff & Hinman, 2021). Here, we use the sea star Patiria miniata as a powerful system to study tubulogenesis within an intact organism.…”

An optimized Tet-On system for conditional control of gene expression in sea urchins

“…Treatment with axitinib, a selective VEGF receptor inhibitor, revealed that VEGF signaling is required for early ingression and also PMC migration and patterning during later stages of development (Adomako-Ankomah and Ettensohn, 2013; Morgulis et al, 2019; Morgulis et al, 2021). Genes with localized expression at the tips of the growing arms are also downregulated in axitinib-treated embryos (Morgulis et al, 2019; Sun and Ettensohn, 2014; Tarsis et al, 2022).…”