Gene expression profiles at different stages for formation of pearl sac and pearl in the pearl oyster Pinctada fucata

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.Electronic supplementary materialThe online version of this article (10.1186/s12864-019-5579-3) contains supplementary material, which is available to authorized users.

Exosome-derived small non-coding RNAs reveal immune response upon grafting transplantation in Pinctada fucata (Mollusca)

“…The shell matrix proteins (SMPs), mostly secreted from OMEs, are directly delivered to the mineralization site via either exosomes or the classical secretory pathway [ 29 , 30 ]. To date, abundant SMPs, which play a vital role in shell and pearl formation, have been identified [ 31 – 33 ]. However, the process by which pearl formation occurs remains poorly understood.…”

“…Currently, most studies on exosomes are primarily focused on their roles in disease and immune response [ 34 , 35 ], while exosomes are also involved in shell and pearl formation in molluscs [ 28 ]. In pearl farming, small pieces of mantle tissue from donor oysters are implanted into the gonad of host oysters along with an inorganic bead (termed the ‘nucleus’) for large-scale production of artificial pearls [ 33 , 36 ]. Surgical implantation of the mantle can induce an immune reaction in response to transplantation for the survival of the host oyster [ 37 ].…”

Pearl Sac Gene Expression Profiles Associated With Pearl Attributes in the Silver-Lip Pearl Oyster, Pinctada maxima

“…The pearl sac first secretes an organic layer onto the surface of the nucleus ( Taylor and Strack, 2008 ). This is followed by the deposition of successive layers of calcium carbonate, first prismatic and then nacreous, although a large degree of variation can be observed in individual pearls ( Cuif et al, 2008 , 2011 ; Mariom et al, 2019 ). This structural layering is similar to that observed within the pearl oyster shell that also consists of three layers; an outer organic-rich layer (the periostracum), a middle prismatic layer of calcite, and an inner nacreous layer of aragonite.…”

“…Gene expression analysis of pearl sacs has revealed that pearl formation also involves many of these previously identified SMPs (Wang et al, 2009;Inoue et al, 2010;McGinty et al, 2012;Zhan et al, 2013;Le Luyer et al, 2019); however, pearl sac specific isoforms of known biomineralization genes have also been reported (Kinoshita et al, 2011). Temporal transcriptomic analysis has further revealed that SMPs associated with the prismatic shell layer are up-regulated in the early stages of pearl formation, whereas those associated with the nacreous shell layer are up-regulated later (Mariom et al, 2019), suggesting that the molecular process of pearl formation largely recapitulates that observed in the shell.…”

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“…The pearl sac first secretes an organic layer onto the surface of the nucleus (Taylor and Strack, 2008). This is followed by the deposition of successive layers of calcium carbonate, first prismatic and then nacreous, although a large degree of variation can be observed in individual pearls (Cuif et al, 2008(Cuif et al, , 2011Mariom et al, 2019). This structural layering is similar to that observed within the pearl oyster shell that also consists of three layers; an outer organic-rich layer (the periostracum), a middle prismatic layer of calcite, and an inner nacreous layer of aragonite.…”