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PfSMAD4 plays a role in biomineralization and can transduce bone morphogenetic protein-2 signals in the pearl oyster Pinctada fucata.

ABSTRACT: Mollusca is the second largest phylum in nature. The shell of molluscs is a remarkable example of a natural composite biomaterial. Biomineralization and how it affects mollusks is a popular research topic. The BMP-2 signaling pathway plays a canonical role in biomineralization. SMAD4 is an intracellular transmitter in the BMP signaling pathway in mammals, and some genomic data show SMAD4's involvement in BMP signaling in invertebrates, but whether SMAD4 plays a conservative role in pearl oyster, Pinctada fucata, still need to be tested.In this study, we identified a SMAD4 gene (hereafter designated PfSMAD4) in pearl oyster Pinctada fucata. Bioinformatics analysis of PfSMAD4 showed high identity with its orthologs. PfSMAD4 was located in the cytoplasm in immunofluorescence assays and analyses of PfSMAD4 mRNA in tissues and developmental stages showed high expression in ovaries and D-shaped larvae. An RNA interference experiment, performed by PfSMAD4 double-stranded RNA (dsRNA) injection, demonstrated inhibition not only of nacre growth but also organic sheet formation with a decrease in PfSMAD4 expression. A knockdown experiment using PfBMP2 dsRNA showed decreased PfBMP2 and PfSMAD4 mRNA and irregular crystallization of the nacreous layer using scanning electron microscopy. In co-transfection experiments, PfBMP2-transactivated reporter constructs contained PfSMAD4 promoter sequences.Our results suggest that PfSMAD4 plays a role in biomineralization and can transduce BMP signals in P. fucata. Our data provides important clues about the molecular mechanisms that regulate biomineralization in pearl oyster.

SUBMITTER: Zhao M

PROVIDER: S-EPMC4845351 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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PfSMAD4 plays a role in biomineralization and can transduce bone morphogenetic protein-2 signals in the pearl oyster Pinctada fucata.

Zhao Mi M Shi Yu Y He Maoxian M Huang Xiande X Wang Qi Q

BMC developmental biology 20160426

<h4>Background</h4>Mollusca is the second largest phylum in nature. The shell of molluscs is a remarkable example of a natural composite biomaterial. Biomineralization and how it affects mollusks is a popular research topic. The BMP-2 signaling pathway plays a canonical role in biomineralization. SMAD4 is an intracellular transmitter in the BMP signaling pathway in mammals, and some genomic data show SMAD4's involvement in BMP signaling in invertebrates, but whether SMAD4 plays a conservative ro ...[more]

PMID: 27113217

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Project description:BackgroundThe molluscan Pinctada fucata is an important pearl-culturing organism to study biomineralization mechanisms. Several biomineralization-related genes play important roles regulating shell formation, but most previous work has focused only on their functions in adult oysters. Few studies have investigated biomineralization during larval development, when the shell is initially constructed and formed until the juvenile stage in dissoconch shells. Here, we report, for the first time, a global gene analysis during larval development of P. fucata based on a microarray and reveal the relationships between biomineralization-related genes and the shell formation process.ResultsBased on the P. fucata mantle transcriptome, 58,940 probes (60 nt), representing 58,623 transcripts, were synthesized. The gene expression profiles of the fertilized egg, trochophore, D-shaped, and umbonal stage larvae, as well as juveniles were analyzed by microarray performance. The expression patterns of the biomineralization-related genes changed corresponding to their regulatory function during shell formation. Matrix proteins chitin synthase and PFMG2 were highly expressed at the D-shaped stage, whereas PFMG6, PFMG8 and PfN23 were significantly up-regulated at the umbonal stage, indicating different roles regulating the formation of either periostracum, Prodissoconch I or Prodissoconch II shells. However, the majority of matrix proteins were expressed at high levels at the juvenile stage, and the shells comprised both an aragonitic nacreous layer and a calcitic prismatic layer as adults. We also identified five new genes that were significantly up-regulated in juveniles. These genes were expressed particularly in the mantle and coded for secreted proteins with tandem-arranged repeat units, as most matrix proteins. RNAi knockdown resulted in disrupted nacreous and prismatic shell layers, indicating their potential roles in shell formation.ConclusionsOur results add a global perspective on larval expression patterns of P. fucata genes and propose a mechanism of how biomineralization-related genes regulate the larval shell formation process. These results increase knowledge about biomineralization-related genes and highlight new aspects of shell formation mechanisms.

Dataset Information

PfSMAD4 plays a role in biomineralization and can transduce bone morphogenetic protein-2 signals in the pearl oyster Pinctada fucata.

Publications

PfSMAD4 plays a role in biomineralization and can transduce bone morphogenetic protein-2 signals in the pearl oyster Pinctada fucata.

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