2019bioRxiv (Cold Spring Harbor Laboratory)Open access

Direct control of shell regeneration by the mantle tissue in the pearl oyster Pinctada fucata via accelerating CaCO3 nucleation

Jingliang Huang, Yangjia Liu, Taifeng Jiang, Wentao Dong, Guilian Zheng, Liping Xie, Rongqing Zhang

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Abstract

Abstract Molluscan bivalves rapidly repair the damaged shells to prevent further injury. However, it remains unclear how this process is precisely controlled. In this study, we applied scanning electronic microscopy, transmission electronic microscopy and histochemical analysis to examine the detailed shell regeneration process of the pearl oyster Pinctada fucata . It was found that the shell damage caused the mantle tissue to retract, which resulted in dislocation of the mantle zones to their correspondingly secreted shell layers. However, the secretory repertoires of the different mantle zones remained unchanged. As a result, the dislocation of the mantle tissue dramatically affected the shell morphology, and the unusual presence of the submarginal zone on the nacreous layers caused de novo precipitation of prismatic layers on the nacreous layers. Real-time PCR revealed that the expression of the shell matrix proteins (SMPs) were significantly upregulated, which was confirmed by the thermal gravimetric analysis (TGA) of the newly formed shell. The increased matrix secretion accelerated CaCO 3 nucleation thus promoting shell deposition. Taken together, our study revealed the close relationship between the physiological activities of the mantle tissue and the morphological change of the regenerated shells.

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Abstract Molluscan bivalves rapidly repair the damaged shells to prevent further injury. However, it remains unclear how this process is precisely controlled. In this study, we applied scanning electronic microscopy, transmission electronic microscopy and histochemical analysis to examine the detailed shell regeneration process of the pearl oyster Pinctada fucata . It was found that the shell damage caused the mantle tissue to retract, which resulted in dislocation of the mantle zones to their correspondingly secreted shell layers. However, the secretory repertoires of the different mantle zones remained unchanged. As a result, the dislocation of the mantle tissue dramatically affected the shell morphology, and the unusual presence of the submarginal zone on the nacreous layers caused de novo precipitation of prismatic layers on the nacreous layers. Real-time PCR revealed that the expression of the shell matrix proteins (SMPs) were significantly upregulated, which was confirmed by the thermal gravimetric analysis (TGA) of the newly formed shell. The increased matrix secretion accelerated CaCO 3 nucleation thus promoting shell deposition. Taken together, our study revealed the close relationship between the physiological activities of the mantle tissue and the morphological change of the regenerated shells.

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Available abstract

Abstract Molluscan bivalves rapidly repair the damaged shells to prevent further injury. However, it remains unclear how this process is precisely controlled. In this study, we applied scanning electronic microscopy, transmission electronic microscopy and histochemical analysis to examine the detailed shell regeneration process of the pearl oyster Pinctada fucata . It was found that the shell damage caused the mantle tissue to retract, which resulted in dislocation of the mantle zones to their correspondingly secreted shell layers. However, the secretory repertoires of the different mantle zones remained unchanged. As a result, the dislocation of the mantle tissue dramatically affected the shell morphology, and the unusual presence of the submarginal zone on the nacreous layers caused de novo precipitation of prismatic layers on the nacreous layers. Real-time PCR revealed that the expression of the shell matrix proteins (SMPs) were significantly upregulated, which was confirmed by the thermal gravimetric analysis (TGA) of the newly formed shell. The increased matrix secretion accelerated CaCO 3 nucleation thus promoting shell deposition. Taken together, our study revealed the close relationship between the physiological activities of the mantle tissue and the morphological change of the regenerated shells.

Key concepts: Pinctada fucata, Mantle (geology), Pearl oyster, Nucleation, Biomineralization, Shell (structure), Bivalvia, Aragonite

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