China is the largest producer of pearls, accounted for over 90% of world’s total pearl production. The triangle sail mussel (Hyriopsis cumingii), the most important species for freshwater pearl culture in China, is a well-known mussel recognized for pearl production with high yield and quality. Here, we reported a high-quality chromosome-level genome assembly of H. cumingii. The size of assembled genome was as large as 3.38 Gb with a scaffold N50 length of 3.19 Mb, and 2.04 Gb genome sequences were anchored onto 19 linkage groups. A total of 37,681 protein-coding genes and 50.86% of repeat elements were predicted and annotated. The expansive of 752 gene families compared to the most closely related Dreissena rostriformis, with a divergence time of 18.5 million years, might reveal an extensive set of genes associated to biomineralization, of which 237 genes were under strong positive selection in H. cumingii genome. Notably, the fibrillin gene family exhibited expansion and positive selection simultaneously, and multiple high expression after mantle implantation, suggesting the reason for outstanding biomineralization ability of H. cumingii. Furthermore, one fibrillin gene was confirmed as involving in deposition of calcium carbonate and formation of amorphous crystal during initial biomineralization based on RNA silencing and In vitro carbonate calcium crystallization assay. Fibrillin genes also diverse our attention from calcium deposition guided by matrix protein to interlamellar membrane configuration for understanding pearl formation. These findings provide a valuable genomic resource for carbonate biomineralization studies and fill the gap on freshwater mussel genome for evolutionary studies.

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