Actomyosin remodeling regulates biomineral formation, growth and morphology during eukaryote skeletogenesis

Abstract

AbstractBiomineralization is believed to have evolved independently in different phyla, using distinct minerals, organic scaffolds and gene regulatory networks (GRNs). Yet, diverse eukaryotes use the actomyosin network in shaping the biomineral, from unicellular organisms, through echinoderm skeletons to vertebrate bones. Specifically, the actomyosin remodeling protein, Rho-associated coiled-coil kinase (ROCK) regulates vertebrates’ chondrocytes, osteoblasts and odontoblasts differentiation and affects gene expression in these biomineralizing cells. Yet, little is known on ROCK role in invertebrates’ biomineralization. Here we reveal that ROCK controls the formation, growth and morphology of the calcite spicules in the sea urchin larva. ROCK expression is elevated in the sea urchin skeletogenic cells and its inhibition impairs the organization of F-actin around the spicules, disrupts skeletogenic gene expression and leads to skeletal loss. ROCK inhibition after spicule formation reduces spicule volume and total length, but not thickness and induces ectopic spicule branching. Similar skeletogenic phenotypes are observed when ROCK is inhibited in a skeletogenic cell culture, indicating that these phenotypes are due to ROCK activity specifically in the skeletogenic cells. We propose that the usage of actomyosin network was employed independently, downstream of convergent GRNs across Eukaryotes, to regulate biomineral growth and morphology.