Abstract

BackgroundThe most critical step in the pearl formation during aquaculture is issued to the proliferation and differentiation of outer epithelial cells of mantle graft into pearl sac. This pearl sac secretes various matrix proteins to produce pearls by a complex physiological process which has not been well-understood yet. Here, we aimed to unravel the genes involved in the development of pearl sac and pearl, and the sequential expression patterns of different shell matrix proteins secreted from the pearl sac during pearl formation by pearl oyster Pinctada fucata using high-throughput transcriptome profiling.ResultsPrincipal component analysis (PCA) showed clearly different gene expression profiles between earlier (before 1 week) and later stages (1 week to 3 months) of grafting. Immune-related genes were highly expressed between 0 h – 24 h (donor dependent) and 48 h – 1 w (host dependent), and in the course of wound healing process pearl sac was developed by two weeks of graft transplantation. Moreover, for the first time, we identified some stem cell marker genes including ABCG2, SOX2, MEF2A, HES1, MET, NRP1, ESR1, STAT6, PAX2, FZD1 and PROM1 that were expressed differentially during the formation of pearl sac. The expression profiling of 192 biomineralization-related genes demonstrated that most of the shell matrix proteins (SMPs) involved in prismatic layer formation were first up-regulated and then gradually down-regulated indicating their involvement in the development of pearl sac and the onset of pearl mineralization. Most of the nacreous layer forming SMPs were up-regulated at 2 weeks after the maturation of pearl sac. Nacrein, MSI7 and shematrin involved in both layer formation were highly expressed during 0 h – 24 h, down-regulated up to 1 week and then up-regulated again after accomplishment of pearl sac formation.ConclusionsUsing an RNA-seq approach we unraveled the expression pattern of the key genes involved in the development of pearl sac and pearl as a result of host immune response after grafting. These findings provide valuable information in understanding the molecular mechanism of pearl formation and immune response in P. fucata.

Highlights

  • The most critical step in the pearl formation during aquaculture is issued to the proliferation and differentiation of outer epithelial cells of mantle graft into pearl sac

  • To know the genes engaged in pearl sac development, we focused on epithelial cell proliferation and differentiation-related Gene ontology (GO) terms

  • We investigated the relative expression patterns of 28 representative shell matrix proteins (SMPs) from 192 biomineralization-related genes having well-defined implications for quality pearl production that are involved in the formation of prismatic layer (10), nacreous layer (14) and both layer (4) (Table 2)

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Summary

Introduction

The most critical step in the pearl formation during aquaculture is issued to the proliferation and differentiation of outer epithelial cells of mantle graft into pearl sac. This pearl sac secretes various matrix proteins to produce pearls by a complex physiological process which has not been well-understood yet. The cells of the pearl sac obtain nourishment from the surrounding haemolymph [8] It takes about 1 to 4 weeks to complete the development of pearl sac depending on several conditions like water temperature [9], season [10], sex of host oyster [11], species [7, 12, 13] and so on. It is very reasonable to claim that pearl sac formation is the most important step of pearl culture that determines the success of culture

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