Possible co-option of a VEGF-driven tubulogenesis program for biomineralization in echinoderms

Abstract

12Biomineralization is the process in which living organisms use minerals to form hard 13 structures that protect and support them. Biomineralization is believed to have evolved 14 rapidly and independently in different phyla utilizing existing components used for other 15 purposes. The mechanistic understanding of the regulatory networks that drive 16 biomineralization and their evolution is far from clear. The sea urchin skeletogenesis is an 17 excellent model system for studying both gene regulation and mineral uptake and deposition. 18The sea urchin calcite spicules are formed within a tubular cavity generated by the 19 skeletogenic cells under the control the vascular endothelial growth factor (VEGF) signaling. 20The VEGF pathway controls tubulogenesis and vascularization across metazoans while its 21 regulation of biomineralization was only observed in echinoderms. Despite the critical role of 22 for vascularization and specifically co-opted for biomineralization in the echinoderm phylum. 33 Significance statement 36The sea urchin calcite spicules and vertebrate blood vessels are quite distinct in their function, 37 yet both have a tubular structure and are controlled by the vascular endothelial growth factor 38 (VEGF) pathway. Here we study the downstream program by which VEGF pathway drives 39 sea urchin spiculogenesis and find remarkable similarities to the control of vertebrate 40 vascularization. The similarities are observed both in the upstream gene regulatory network, 41 in the downstream effector genes and the cellular processes that VEGF signaling controls at 42 the site of the calcite spicule formation. We speculate that sea urchin spiculogenesis and 43 vertebrate vascularization diverged from a common ancestral tubulogenesis program that was 44 co-opted for biomineralization in the echinoderm phylum. 45 46 3 47

The ‘biomineralization toolkit’ and the origin of animal skeletons

“…Intriguingly, the echinoderm skeleton may provide an alternative model for co-option playing a role in the origin of animal biomineralization, with its origin in nutrient or blood collection and transport. Morgulis et al (2019) identify five transcription factors and three signalling pathways involved in vascular endothelial growth factor (VEGF) signalling that are common to biomineralization in echinoderms and vascular tubulogenesis in vertebrates. They find common cytoskeletal remodelling proteins essential for echinoderm spicule formation and the formation of vertebrate vascular tubesstructures with similar overall geometry but fundamentally different functions.…”

“…The diagnostic structure of stereom, the calcium carbonate mineral that comprises the echinoderm skeleton, is common to all five modern classes of echinoderm, along with fossil representatives. However, the larval echinoderm skeleton is not so widespread, being either lost in asteroids and much reduced in holothurians or independently evolved in echinoids and ophiuroids (Raff & Byrne, 2006;Cary & Hinman, 2017 ; Morgulis et al, 2019). Developmental evidence suggests that a common set of transcription factors are involved in adult skeletogenesis in all echinoderms, and some used in the developing larval skeleton evolved at the base of the phylum.…”

“…Developmental evidence suggests that a common set of transcription factors are involved in adult skeletogenesis in all echinoderms, and some used in the developing larval skeleton evolved at the base of the phylum. Clade‐specific parts of the regulatory network may have evolved in echinoids and ophiuroids during the independent evolution of the larval skeleton (Cary & Hinman, 2017; Morgulis et al, 2019) however more recent evidence supports the loss of the asteroid larval skeleton rather than independent origins in other groups (Erkenbrack & Thompson, 2019). The rare aragonitic epidermal ossicles of hemichordates also appear to be independently derived from other deuterostome skeletons (Cameron & Bishop, 2012), with several unique biomineralization genes in the enteropneust Saccoglossus kowalevskii , while still sharing carbonic anhydrase involved in biomineralization with the sea urchin Strongylocentrotus purpuratus .…”

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

“…Biomineralization is the process in which organisms from the five kingdoms of life, use minerals to produce shells, skeletons and teeth that protect and support them (1)(2)(3)(4). Recent studies suggest that biomineralization evolved by the phylum specific co-option of ancestral gene regulatory networks (GRNs) that drove the construction of distinct organic scaffolds (4)(5)(6)(7)(8)(9) and by the evolution of specialized sets of biomineralization proteins (3,7,(10)(11)(12)(13)). This explanation is in line with the dissimilar GRNs and biomineralization proteins that drive biomineralization in different phyla (5,12,14).…”

Worms and gills, plates and spines: the evolutionary origins and incredible disparity of deuterostomes revealed by fossils, genes, and development

“…This reversed Cambrian record might suggest that biomineralization could have evolved independently in multiple lineages, with radially symmetric echinoderms biomineralizing the skeleton first. However, although skeleton biomineralization occurred independently throughout the metazoan tree as a result of reutilization of developmental networks (Erwin et al, 2011;Morgulis et al, 2019;Murdock, 2020), the intricate nature of the echinoderm stereom strongly supports a single origination. As a result, a unique evolution of echinoderm biomineralization prior to Stage 3 suggests that echinoderms would have exhibited extremely high rates of morphological evolution , which means that radially symmetric echinoderms (not only helicoplacoids, but also the pentaradial 'eocrinoids') would have evolved within 10-15 million years after the origin of the phylum.…”