Ben-Tabou de-Leon S (2022), The Evolution of Biomineralization through the ...

ECB-ART-50471

Cells 2022 Feb 09;114:. doi: 10.3390/cells11040595.

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The Evolution of Biomineralization through the Co-Option of Organic Scaffold Forming Networks.

Ben-Tabou de-Leon S .

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Biomineralization is the process in which organisms use minerals to generate hard structures like teeth, skeletons and shells. Biomineralization is proposed to have evolved independently in different phyla through the co-option of pre-existing developmental programs. Comparing the gene regulatory networks (GRNs) that drive biomineralization in different species could illuminate the molecular evolution of biomineralization. Skeletogenesis in the sea urchin embryo was extensively studied and the underlying GRN shows high conservation within echinoderms, larval and adult skeletogenesis. The organic scaffold in which the calcite skeletal elements form in echinoderms is a tubular compartment generated by the syncytial skeletogenic cells. This is strictly different than the organic cartilaginous scaffold that vertebrates mineralize with hydroxyapatite to make their bones. Here I compare the GRNs that drive biomineralization and tubulogenesis in echinoderms and in vertebrates. The GRN that drives skeletogenesis in the sea urchin embryo shows little similarity to the GRN that drives bone formation and high resemblance to the GRN that drives vertebrates' vascular tubulogenesis. On the other hand, vertebrates' bone-GRNs show high similarity to the GRNs that operate in the cells that generate the cartilage-like tissues of basal chordate and invertebrates that do not produce mineralized tissue. These comparisons suggest that biomineralization in deuterostomes evolved through the phylum specific co-option of GRNs that control distinct organic scaffolds to mineralization.

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	Figure 1. Partial Eumetazoan phylogenetic tree containing phyla and species discussed in this paper and their biomineralization programs. (A), calcification in cnidarian and protostome phyla. Numbers in red is the estimated time of divergence in million years (MA) based on [27,29]. Light blue indicates the usage of different CaCO3 polymorphs including but not limited to calcite, aragonite or vaterite. Dark blue indicates the usage of calcite, and purple indicates the usage of apatite. Black indicates non-mineralizing species. (B), skeleton formation in deuterostomes. Color code as in (A), with the addition of green, indicating the usage of cartilage by the skeletogenic tissue. Squares indicate the evolutionary origin of a specific skeletal tissue.
	Figure 2. Possible models for the evolution of biomineralization GRNs from ancestral GRNs. (A), a model where an ancestral GRN that drove the formation of an organic scaffold was co-opted for biomineralization by activating regulatory and differentiation genes that assist in calcification. In this model we expect to see a strong similarity between the biomineralization of GRN to the GRN that drive the formation of the organic scaffold in non-biomineralization species. (B), a model where an ancestral GRN that drove the activation of genes that participate in calcification was co-opted for biomineralization through the activation of phylum specific regulatory and differentiation genes that control organic scaffold formation. In that case, we expect to see a similarity between the regulatory and differentiation genes that drive calcification in the two phyla.
	Figure 3. Sea urchin skeletogenic GRN and the evolution of echinoderm skeletogenic GRN. (A), a scheme showing larval skeleton formation in the sea urchin embryo. The skeletogenic cells (red) form a ring with two lateral skeletogenic clusters where the spicule form. Enlargement, showing the mineral (gray) concentrated in vesicles and transported to the spicule tubular compartment where it is engulfed within a thin layer of extracellular matrix. (B), sea urchin larval skeletogenic GRN and differentiation genes with various functions. (C–E), embryonic territories in the different echinoderm clades. Color codes are explained in the figure and in the text. C, embryonic territories in the sea urchin (SU) and the pencil sea urchin (PU). D, embryonic territories in the sea cucumber (SC) and brittle star (BS). (E), embryonic territories in the sea star (SS). (F), expression of the skeletogenic regulatory genes in the mesoderm of embryos of different echinoderm clades. Color code explained in figure. (G), expression of skeletogenic regulatory genes in adult skeletogenic cells in three echinoderm clades.
	Figure 4. Bone biomineralization and vascular tubulogenesis GRNs in vertebrates. (A), schematic diagram showing a cross section of the dorsal part of a vertebrate embryo and the different embryonic territories that contribute to skeletal and vascular tissues. (B), tissues and cell types that participate in endochondral ossification in vertebrates. Immature cartilage (green) is generated by proliferating and resting chondrocytes. Mature cartilage (blue) is generated by hypertrophic chondrocytes, bone matrix and mineralization (gray) are generated by osteoblasts, maintained by osteocytes and reabsorbed by osteoclasts (purple). (C), GRN and differentiation genes in the different bone forming cells. Color code matches the territories and cells in (B,D), schematic diagram of vertebrate blood vessel showing the different cell types that constitute it. Blood cells occupy the lumen which is engulfed by endothelial cells. The endothelial cells are bound to the basement membrane from the inner side of the vessel and pericytes from the outside. Image courtesy of Yarden Ben-Tabou de-Leon (artist). (E), endothelial cell GRN and differentiation genes.
	Figure 5. Proposed models of the evolution of the biomineralization GRNs in echinoderms and in vertebrates. (A), an ancestral vascular GRN that generated blood vessels where hemocytes flow evolved in vertebrates to make the endothelial GRN and was co-opted for biomineralization in echinoderms. The ancestral vascular GRN included the VEGF pathway and transcription factors of the ETS family. Co-option for biomineralization included the activation of the transcription factor Alx1, the evolution of novel echinoderm spicule matrix (SM) proteins and the activation of genes of the biomineralization toolkit. The vertebrate endothelial GRN and the echinoderm skeletogenic GRN show similarities and trans-differentiation potential to the hemocyte GRN. (B), an ancestral GRN that drove cartilage formation was co-opted for biomineralization in the vertebrate phylum. The ancestral cartilage GRN included the transcription factors SoxE and SoxD that drove the expression of Col2. The co-option for biomineralization was through the activation of the transcription factors Runx and Sp7, the evolution of novel bone matrix (BM) proteins and the activation of Col1 and genes of the biomineralization toolkit.

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Adomako-Ankomah, Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation. 2013, Pubmed, Echinobase