Sci Rep 2024 Nov 18;141:28525. doi: 10.1038/s41598-024-76239-7.

Structural and molecular distinctions of primary and secondary spines in the sea urchin Lytechinus variegatus.

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Sea urchins (echinoids) are common model organisms for research in developmental biology and for their unusual transition from a bilaterally organized larva into a post-metamorphic adult with pentaradial body symmetry. The adult also has a calcareous endoskeleton with a multimetameric pattern of continuously added elements, among them the namesake of this phylum, spines. Nearly all echinoids have both large primary spines, and an associated set of smaller secondary spines. We hypothesize that the secondary spines of the tropical variegated urchin species, Lytechinus variegatus, are morphologically and molecularly distinct structures from primary spines and not just small versions of the large spines. To test this premise, we examined both spine types using light microscopy, micro-CT imaging, lectin labeling, transcriptomics, and fluorescence in situ hybridization (FISH). Our findings reveal basic similarities between the two spine types in mineral and cellular anatomy, but with clear differences in growth patterns, genes expressed, and in the profile of various expressed genes. In particular, secondary spines have non-overlapping, longitudinally concentrated growth bands that lead to a blunt and straight profile, and a distinct transcriptome involving the upregulation in many genes in comparison to the primary spines. Neural, ciliary, and extracellular matrix interacting factors are implicated in the differentially expressed gene (DEG) dataset, including two genes-ONECUT2 and an uncharacterized discoidin- and thrombospondin-containing protein. We show spine type-specific localizations by FISH, which will be of interest to ongoing work in urchin spine patterning. These results demonstrate that primary and secondary spines of L. variegatus have overlapping but distinct molecular and biomineralization characteristics, suggesting unique developmental, regenerative, and representation in this spiny dermal phylum.

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