Genome-wide association study analysis to resolve the key regulatory mechanism of biomineralization in Pinctada fucata martensii

Biomineralization-controlled exo-/endoskeleton growth contributes to body growth and body size diversity. Molluscan shells undergo ectopic biomineralization to form the exoskeleton and biocalcified pearl involved in invading defence. Notably, exo-/endoskeletons have a common ancestral origin, but their regulation and body growth are largely unknown. This study employed the pearl oyster, Pinctada fucata marntensii, a widely used experimental model for biomineralization in invertebrates, to perform whole-genome resequencing of 878 individuals from wild and breeding populations. This study characterized the genetic architecture of biomineralization-controlled growth and ectopic biomineralization. The insulin-like growth factor (IGF) endocrine signal interacted with ancient single-copy transcription factors to form the regulatory network. Moreover, the cross-phylum regulation of key long noncoding RNA (lncRNA) in bivalves and mammals indicated the conserved genetic and epigenetic regulation in exo-/endoskeleton growth. Thyroid hormone signal and apoptosis regulation in pearl oysters affected ectopic biomineralization in pearl oyster. These findings provide insights into the mechanism underlying the evolution and regulation of biomineralization in exo-/endoskeleton animals and ectopic biomineralization.

Automated summary

Biomineralization-controlled growth of exo-/endoskeleton contributes to body growth and size diversity. This study used pearl oysters to investigate the genetic regulation of biomineralization-controlled growth and ectopic biomineralization. The insulin-like growth factor (IGF) endocrine signal and ancient single-copy transcription factors formed the regulatory network. Cross-phylum regulation of key long noncoding RNA (lncRNA) in bivalves and mammals suggests conserved genetic and epigenetic regulation. Thyroid hormone signal and apoptosis regulation affected ectopic biomineralization in pearl oysters.