Abstract
Immune response plays an important role in the pearl sac formation and pearl quality. However, there is little knowledge about the mode and mechanism of the immune responses in the pearl sac formation of H. cumingii, which produced the largest production of non-nucleated freshwater pearl in China. In this study, we monitored the process of pearl sac formation by histology examination for 18 days after grafting. The results showed that a large number of hemocytes aggregated in the pearl sac cavity on day 8 after grafting and provided organic substrate for the deposition of extracellular matrix and CaCO3 crystal and mediated the initiation of pearl forming on day 12. These results revealed the important role of hemocytes on the early pearl sac and pearl formations. In the transcriptome analysis of pearl sac at the key time points of day 0 and day 6, 8, 12 after grafting, the expression profiles of the immune-related genes revealed the immune response pattern of H. cumingii after grafting. The significant up-regulation of the hydrolytic enzymes, acute phase proteins, and antimicrobial peptides of humoral defense factors on day 6 after grafting suggested that these immune-related gene products were the main immune defense during the early wound healing; Meanwhile, the continuous up-regulation of antioxidant enzymes such as Cu-Zn SOD, Se-GPX, and tyrosinase in prophenoloxidase (proPO) system on day 8 and day 12 suggested the important role of these immune effectors in oxidation-reduction on the later stage of pearl sac and pearl formations in H. cumingii. Moreover, the results of KEGG analysis of differentially expressed genes suggested the potential regulatory function of the signaling pathways of proPO system and complement system during pearl sac formation. These results provided valuable new insights into the roles and functions of the immune system in pearl sac and pearl formation.
Highlights
Pearl is one of the expensive organic jewelry and is used as a precious traditional Chinese medicine
During the process of pearl sac formation, the saibo was clearly free in the incision site of mantle connective tissue of host mussel on days 2 to 6 after grafting (Figures 1A–C); the connective tissue of saibo gradually integrated with the connective tissue of the host mussel on days 8 to 10 after grafting (Figures 2A,B), and the integration was full completed on day 12 after grafting (Figure 2C)
Histological analysis showed that there were three important time points in the process of wound healing and pearl sac formation in H. cumingii, which included (1) days 6 to 8 after grafting when the saibo integrated into the mantle connective tissue of the host mussel (Figure 1C) (2) days 8 to 10 after grafting when a large number of hemocytes aggregated in the pearl sac cavity (Figures 2A,B), and (3) day 12 after grafting when CaCO3 crystals were formed in the hemocytes clots and the epithelial cells of the pearl sac began to secrete extracellular matrix to mediate further CaCO3 crystal deposition (Figures 2F, 3)
Summary
Pearl is one of the expensive organic jewelry and is used as a precious traditional Chinese medicine. The immune response remains active during the process of pearl sac formation to tolerate the nucleus and allograft implantation (Li et al, 2010; Kishore and Southgate, 2015a; Wang W. et al, 2017). Excessive inflammatory reaction will increase the nucleus rejection and mortality in the marine pearl oysters Pinctada margaritifera and P. maxima (CochennecLaureau et al, 2010) and the freshwater pearl mussel H. cumingii (Li et al, 2010). Histological analysis showed that at the initiation of pearl sac formation, a large number of hemocytes accumulated at the incision site to seal the damaged area and triggered the subsequent immune process of wound healing (Li et al, 2010; Kishore and Southgate, 2015b). The hemocytes, initially surrounding in the pearl sac, would infiltrate into the nucleus cavity (Acosta-Salmon and Southgate, 2006; Eddy et al, 2015; Atsumi et al, 2018), but the excessive accumulation of hemocytes could cause bulges in the pearl sac, resulting in an irregularly shaped pearl (Kishore and Southgate, 2015a)
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