Abstract:The highly recognizable animals within the phylum Echinodermata encompass an enormous disparity of adult and larval body plans. The extensive knowledge of sea urchin development has culminated in the description of the exquisitely detailed gene regulatory network (GRN) that governs the specification of various embryonic territories. This information provides a unique opportunity for comparative studies in other echinoderm taxa to understand the evolution and developmental mechanisms underlying body plan change… Show more
“…While all echinoderm classes generate calcite endoskeletons in their adult form (17), some echinoderm classes lack the larval skeleton (sea stars) or have a significantly reduced skeletal structure [sea cucumbers (17)]. Nevertheless, the embryonic mesodermal GRN is highly similar in all echinoderm classes, regardless of the presence or absence of a larval skeleton (18). Indeed, VEGFR expression is one of the only differences in the mesoderm regulatory state between echinoderm embryos that produce larval skeletons [brittle stars and sea urchins (14,19)] and the sea star embryo, which does not (14,15,(18)(19)(20)(21).…”
Biomineralization is the process by which living organisms use minerals to form hard structures that protect and support them. Biomineralization is believed to have evolved rapidly and independently in different phyla utilizing preexisting components. The mechanistic understanding of the regulatory networks that drive biomineralization and their evolution is far from clear. Sea urchin skeletogenesis is an excellent model system for studying both gene regulation and mineral uptake and deposition. The sea urchin calcite spicules are formed within a tubular cavity generated by the skeletogenic cells controlled by vascular endothelial growth factor (VEGF) signaling. The VEGF pathway is essential for biomineralization in echinoderms, while in many other phyla, across metazoans, it controls tubulogenesis and vascularization. Despite the critical role of VEGF signaling in sea urchin spiculogenesis, the downstream program it activates was largely unknown. Here we study the cellular and molecular machinery activated by the VEGF pathway during sea urchin spiculogenesis and reveal multiple parallels to the regulation of vertebrate vascularization. Human VEGF rescues sea urchin VEGF knockdown, vesicle deposition into an internal cavity plays a significant role in both systems, and sea urchin VEGF signaling activates hundreds of genes, including biomineralization and interestingly, vascularization genes. Moreover, five upstream transcription factors and three signaling genes that drive spiculogenesis are homologous to vertebrate factors that control vascularization. Overall, our findings suggest that sea urchin spiculogenesis and vertebrate vascularization diverged from a common ancestral tubulogenesis program, broadly adapted for vascularization and specifically coopted for biomineralization in the echinoderm phylum.
“…While all echinoderm classes generate calcite endoskeletons in their adult form (17), some echinoderm classes lack the larval skeleton (sea stars) or have a significantly reduced skeletal structure [sea cucumbers (17)]. Nevertheless, the embryonic mesodermal GRN is highly similar in all echinoderm classes, regardless of the presence or absence of a larval skeleton (18). Indeed, VEGFR expression is one of the only differences in the mesoderm regulatory state between echinoderm embryos that produce larval skeletons [brittle stars and sea urchins (14,19)] and the sea star embryo, which does not (14,15,(18)(19)(20)(21).…”
Biomineralization is the process by which living organisms use minerals to form hard structures that protect and support them. Biomineralization is believed to have evolved rapidly and independently in different phyla utilizing preexisting components. The mechanistic understanding of the regulatory networks that drive biomineralization and their evolution is far from clear. Sea urchin skeletogenesis is an excellent model system for studying both gene regulation and mineral uptake and deposition. The sea urchin calcite spicules are formed within a tubular cavity generated by the skeletogenic cells controlled by vascular endothelial growth factor (VEGF) signaling. The VEGF pathway is essential for biomineralization in echinoderms, while in many other phyla, across metazoans, it controls tubulogenesis and vascularization. Despite the critical role of VEGF signaling in sea urchin spiculogenesis, the downstream program it activates was largely unknown. Here we study the cellular and molecular machinery activated by the VEGF pathway during sea urchin spiculogenesis and reveal multiple parallels to the regulation of vertebrate vascularization. Human VEGF rescues sea urchin VEGF knockdown, vesicle deposition into an internal cavity plays a significant role in both systems, and sea urchin VEGF signaling activates hundreds of genes, including biomineralization and interestingly, vascularization genes. Moreover, five upstream transcription factors and three signaling genes that drive spiculogenesis are homologous to vertebrate factors that control vascularization. Overall, our findings suggest that sea urchin spiculogenesis and vertebrate vascularization diverged from a common ancestral tubulogenesis program, broadly adapted for vascularization and specifically coopted for biomineralization in the echinoderm phylum.
The skeletogenic gene regulatory network (GRN) of sea urchins and other echinoderms is one of the most intensively studied transcriptional networks in any developing organism. As such, it serves as a pre-eminent model of GRN architecture and evolution. This review summarizes our current understanding of this developmental network. We describe in detail the most comprehensive model of the skeletogenic GRN, one developed for the euechinoid sea urchin Strongylocentrotus purpuratus, including its initial deployment by maternal inputs, its elaboration and stabilization through regulatory gene interactions, and its control of downstream effector genes that directly drive skeletal morphogenesis. We highlight recent comparative studies that have leveraged the euechinoid GRN model to examine the evolution of skeletogenic programs in diverse echinoderms, studies that have revealed both conserved and divergent features of skeletogenesis within the phylum. Lastly, we summarize the major insights that have emerged from analysis of the structure and evolution of the echinoderm skeletogenic GRN and identify key, unresolved questions as a guide for future work.
“…Our present understanding of echinoderm neural development is mainly derived from studies on the Eleutherozoa (Byrne, Nakajima, Chee, & Burke, 2007;Cary & Hinman, 2017;Hirokawa, Komatsu, & Nakajima, 2008;Katow et al, 2010;Nakano, Murabe, Amemiya, & Nakajima, 2006) and much less information is available on crinoid neural development. Indeed, despite their key phylogenetic position, crinoids have been scarcely exploited in both developmental and evolutionary studies and only recently interest in crinoid developmental processes has aroused (Amemiya et al, 2015;Comeau, Bishop, & Cameron, 2017;Nakano, Nakajima, & Amemiya, 2009;Omori, Akasaka, Kurokawa, & Amemiya, 2011).…”
Neural development of echinoderms has always been difficult to interpret, as larval neurons degenerate at metamorphosis and a tripartite nervous system differentiates in the adult. Despite their key phylogenetic position as basal echinoderms, crinoids have been scarcely studied in developmental research. However, since they are the only extant echinoderms retaining the ancestral body plan of the group, crinoids are extremely valuable models to clarify neural evolution in deuterostomes. Antedon mediterranea is a feather star, endemic to the Mediterranean Sea. Its development includes a swimming lecithotrophic larva, the doliolaria, with basiepithelial nerve plexus, and a sessile filter‐feeding juvenile, the pentacrinoid, whose nervous system has never been described in detail. Thus, we characterized the nervous system of both these developmental stages by means of immunohistochemistry and, for the first time, in situ hybridization techniques. The results confirmed previous descriptions of doliolaria morphology and revealed that the larval apical organ contains two bilateral clusters of serotonergic cells while GABAergic neurons are localized under the adhesive pit. This suggested that different larval activities (e.g., attachment and metamorphosis) are under the control of different neural populations. In pentacrinoids, the analysis showed the presence of a cholinergic entoneural system while the ectoneural plexus appeared more composite, displaying different neural populations. The expression of three neural‐related microRNAs was described for the first time, suggesting that these are evolutionarily conserved also in basal echinoderms. Overall, our results set the stage for future investigations that will reveal new information on echinoderm evo‐devo neurobiology.
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