Abstract
Simple SummaryMetamorphosis, the process by which the young forms of some animals develop into adult forms, has long kept scientists on tenterhooks. Flatfish undergo one of the most dramatic metamorphoses described in the entire animal kingdom, in which a symmetrical larva that swims upright and looks just like a typical baby fish becomes a completely flat, asymmetrical juvenile that will live its entire adult life attached to the bottom. To answer the question of how the same organism can generate two completely different body plans associated with different phases of the life cycle, we investigated the dynamics of the brain transcriptome, which is the regulatory center of specific endocrine-activated developmental processes during metamorphosis. Our results show, for the first time, a temporary immune system reorganization during flatfish metamorphic remodelling process. Therefore, characterizing and understanding all the developmental changes that take place during metamorphosis will assist in the understanding the importance of each of these processes in the normal development of an individual and therefore, facilitate the transfer of knowledge to prevent abnormal development or developmental pathologies.Metamorphosis is a captivating process of change during which the morphology of the larva is completely reshaped to face the new challenges of adult life. In the case of fish, this process initiated in the brain has traditionally been considered to be a critical rearing point and despite the pioneering molecular work carried out in other flatfishes, the underlying molecular basis is still relatively poorly characterized. Turbot brain transcriptome of three developmental stages (pre-metamorphic, climax of metamorphosis and post-metamorphic) were analyzed to study the gene expression dynamics throughout the metamorphic process. A total of 1570 genes were differentially expressed in the three developmental stages and we found a specific pattern of gene expression at each stage. Unexpectedly, at the climax stage of metamorphosis, we found highly expressed genes related to the immune response, while the biological pathway enrichment analysis in pre-metamorphic and post-metamorphic were related to cell differentiation and oxygen carrier activity, respectively. In addition, our results confirm the importance of thyroid stimulating hormone, increasing its expression during metamorphosis. Based on our findings, we assume that immune system activation during the climax of metamorphosis stage could be related to processes of larval tissue inflammation, resorption and replacement, as occurs in other vertebrates.
Highlights
Metamorphosis is a post-embryonic process that involves radical changes in morphology, physiology and habitat, leading to stage-specific organs and structures [1]
biological process (BP) ontologies related to immune system processes, such as antigen processing and presentation of endogenous peptide antigen via MHC class I (GO:00019885), innate immune response (GO:0045087) and immune response (GO:0006958), in molecular function (MF) category the most significant Gene Ontology (GO) terms were NAD+ ADP-ribosyltransferase activity (GO:0003950), extracellular matrix structural constituent (GO:0005201) and protein transmembrane transporter activity (GO:0008320) and in the cellular component (CC) category we found ontologies such as collagen trimer (GO:0005581), collagen type I primer (GO:0005584) and extracellular matrix (GO:0031012)
Our results show a clear and evident reorganization of the immune system during the metamorphosis process of flatfish
Summary
Metamorphosis is a post-embryonic process that involves radical changes in morphology, physiology and habitat, leading to stage-specific organs and structures [1]. Most teleost fish undergo metamorphosis in the transition from larva to juvenile stage [8,9]; the most dramatic metamorphosis known in fish is that of flatfish (order Pleuronectiformes) [10], which includes species of high economic value such as turbot (Scophthalmus maximus), Senegalese sole (Solea senegalensis) or Atlantic halibut (Hippoglossus hippoglossus). A pelagic and bilateral symmetric larva becomes a benthonic asymmetric juvenile. Profound internal and external changes, such as eye migration to the opposite side of the body, remodelling of the craniofacial complex [11,12,13] and redistribution of the skin pigmentation [14], lead to an asymmetric juvenile fish adapted to benthic life
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