Transcriptional regulation analysis reveals the complexity of metamorphosis in the Pacific oyster (Crassostrea gigas)

Many marine invertebrate phyla are characterized by indirect development. These animals transit from planktonic larvae to benthic spats via settlement and metamorphosis, which contributes to their adaption to the marine environment. Studying the biological process of metamorphosis is, thus, key to understanding the origin and evolution of indirect development. Although numerous studies have been conducted on the relationship between metamorphosis and the marine environment, microorganisms, and neurohormones, little is known about gene regulation network (GRN) dynamics during metamorphosis. Metamorphosis-competent pediveligers of the Pacific oyster Crassostrea gigas were assayed in this study. By assaying gene expression patterns and open chromatin region changes of different samples of larvae and spats, the dynamics of molecular regulation during metamorphosis were examined. The results indicated significantly different gene regulation networks before, during and post-metamorphosis. Genes encoding membrane-integrated receptors and those related to the remodeling of the nervous system were upregulated before the initiation of metamorphosis. Massive biogenesis, e.g., of various enzymes and structural proteins, occurred during metamorphosis as inferred from the comprehensive upregulation of the protein synthesis system post epinephrine stimulation. Hierarchical downstream gene networks were then stimulated. Some transcription factors, including homeobox, basic helix–loop–helix and nuclear receptors, showed different temporal response patterns, suggesting a complex GRN during the transition stage. Nuclear receptors, as well as their retinoid X receptor partner, may participate in the GRN controlling oyster metamorphosis, indicating an ancient role of the nuclear receptor regulation system in animal metamorphosis.