Genome-wide identification and characterization of Pif genes in the Yesso scallop (Patinopecten yessoensis), and their expression patterns in response to Polydora shell infestation

Abstract

Abstract Pif is an acid matrix protein that is known to be a key macromolecule in the shell nacre formation of molluscs. However, the investigation into the Pif gene at the whole genome level has seldom been carried out, limiting the systematic understanding of its evolution and function. The Yesso scallop (Patinopecten yessoensis), an ancient bivalve with important economic value and evolutionary status, has suffered severe shell infestation by Polydora that badly damaged shell structures. In this study, a total of eight Pif homologous genes (PyPif1–7 and PyBMSP) were identified in the whole genome of the Yesso scallop with diverse gene structures. Two conserved functional domains, VWA and chitin-binding domains, were detected in all PyPif proteins, although with variation in number of copies. Phylogenetic analysis of the Pifs among different molluscan species suggested the molecular evolution of Pif genes was consistent with taxonomic relationships. High sequence divergence of Pif proteins existed among the different species, but a high level of similarity was found in BMSPs, which own four VWA domains. High expression levels of PyBMSP in the central mantles of the healthy and Polydora shell infested Yesso scallops indicated its important role in shell formation. The other PyPifs (PyPif2, PyPif3, PyPif4, PyPif5, PyPif6) may function when the shell is injured, as significantly increased expression levels of these genes were found in the edge mantles of the infested scallops. In addition, haemocytes may also participate in shell repair by up-regulating the expression of PyPifs. This study provides new insights into the evolution and expression patterns of Pif genes in molluscs, which are valuable for elucidating the mechanism of shell repair and formation.