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- Domain-dependent evolution explains functional homology of protostome and deuterostome complement C3-like proteinsPublication . Peng, Maoxiao; Li, Zhi; Cardoso, João; Niu, Donghong; Liu, Xiaojun; Dong, Zhiguo; Li, Jiale; Power, DeborahComplement proteins emerged early in evolution but outside the vertebrate clade they are poorly characterized. An evolutionary model of C3 family members revealed that in contrast to vertebrates the evolutionary trajectory of C3-like genes in cnidarian, protostomes and invertebrate deuterostomes was highly divergent due to independent lineage and species-specific duplications. The deduced C3-like and vertebrate C3, C4 and C5 proteins had low sequence conservation, but extraordinarily high structural conservation and 2-chain and 3-chain protein isoforms repeatedly emerged. Functional characterization of three C3-like isoforms in a bivalve representative revealed that in common with vertebrates complement proteins they were cleaved into two subunits, b and a, and the latter regulated inflammation-related genes, chemotaxis and phagocytosis. Changes within the thioester bond cleavage sites and the a-subunit protein (ANATO domain) explained the functional differentiation of bivalve C3-like. The emergence of domain-related functions early during evolution explains the overlapping functions of bivalve C3-like and vertebrate C3, C4 and C5, despite low sequence conservation and indicates that evolutionary pressure acted to conserve protein domain organization rather than the primary sequence.
- Evolution and potential function in molluscs of neuropeptide and receptor homologues of the insect allatostatinsPublication . Li, Zhi; Cardoso, João; Peng, Maoxiao; Inácio, João P. S.; Power, DeborahThe allatostatins (ASTs), AST-A, AST-B and AST-C, have mainly been investigated in insects. They are a large group of small pleotropic alloregulatory neuropeptides that are unrelated in sequence and activate receptors of the rhodopsin G-protein coupled receptor family (GPCRs). The characteristics and functions of the homologue systems in the molluscs (Buccalin, MIP and AST-C-like), the second most diverse group of protostomes after the arthropods, and of high interest for evolutionary studies due to their less rearranged genomes remains to be explored. In the present study their evolution is deciphered in molluscs and putative functions assigned in bivalves through meta-analysis of transcriptomes and experiments. Homologues of the three arthropod AST-type peptide precursors were identified in molluscs and produce a larger number of mature peptides than in insects. The number of putative receptors were also distinct across mollusc species due to lineage and species-specific duplications. Our evolutionary analysis of the receptors identified for the first time in a mollusc, the cephalopod, GALR-like genes, which challenges the accepted paradigm that AST-AR/buccalin-Rs are the orthologues of vertebrate GALRs in protostomes. Tissue transcriptomes revealed the peptides, and their putative receptors have a widespread distribution in bivalves and in the bivalve Mytilus galloprovincialis, elements of the three peptide-receptor systems are highly abundant in the mantle an innate immune barrier tissue. Exposure of M. galloprovincialis to lipopolysaccharide or a marine pathogenic bacterium, Vibrio harveyi, provoked significant modifications in the expression of genes of the peptide precursor and receptors of the AST-C-like system in the mantle suggesting involvement in the immune response. Overall, our study reveals that homologues of the arthropod AST systems in molluscs are potentially more complex due to the greater number of putative mature peptides and receptor genes. In bivalves they have a broad and varying tissue distribution and abundance, and the elements of the AST-C-like family may have a putative function in the immune response.
- Revisiting the evolution of family B1 GPCRs and ligands: insights from molluscaPublication . Cardoso, João; Mc Shane, Jennifer; Li, Zhi; Peng, Maoxiao; Power, Deborah MaryFamily B1 G protein-coupled receptors (GPCRs) are one of the most well studied neuropeptide receptor families since they play a central role in many biological processes including endocrine, gastrointestinal, cardiovascular and reproduction in animals. The genes for these receptors emerged from a common ancestral gene in bilaterian genomes and evolved via gene/genome duplications and deletions in vertebrate and invertebrate genomes. Their existence and function have mostly been characterized in vertebrates and few studies exist in invertebrate species. Recently, an increased interest in molluscs, means a series of genomes have become available, and since they are less modified than insect and nematode genomes, they are ideal to explore the origin and evolution of neuropeptide gene families. This review provides an overview of Family B1 GPCRs and their peptide ligands and incorporates new data obtained from Mollusca genomes and taking a comparative approach challenges existing models on their origin and evolution.
- Neuropeptides regulate shell growth in the Mediterranean mussel (Mytilus galloprovincialis).Publication . Li, Zhi; Peng, Maoxiao; Félix, Rute; Cardoso, João; Power, Deborah MaryIn bivalves, which are molluscs enclosed in a biomineralized shell, a diversity of neuropeptide precursors has been described but their involvement in shell growth has been largely neglected. Here, using a symmetric marine bivalve, the Mediterranean mussel (Mytilus galloprovincialis), we uncover a role for the neuroendocrine system and neuropeptides in shell production. We demonstrate that the mantle is rich in neuropeptide precursors and that a complex network of neuropeptide-secreting fibres innervates the mantle edge a region highly involved in shell growth. We show that shell damage and shell repair significantly modify neuropeptide gene expression in the mantle edge and the nervous ganglia (cerebropleural ganglia, CPG). When the CPG nerve commissure was severed, shell production was impaired after shell damage, and modified neuropeptide gene expression, the spatial organization of nerve fibres in the ganglia and mantle and biomineralization enzyme activity in the mantle edge. Injection of CALCIa and CALCIIa peptides rescued the impaired shell repair phenotype providing further support for their role in biomineralization. We propose that the regulatory mechanisms identified are likely to be conserved across bivalves and other shelled molluscs since they all share a similar nervous system, a common mantle biomineralization toolbox, and shell structure.