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      Specific Gene Expression Responses to Parasite Genotypes Reveal Redundancy of Innate Immunity in Vertebrates

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          Abstract

          Vertebrate innate immunity is the first line of defense against an invading pathogen and has long been assumed to be largely unspecific with respect to parasite/pathogen species. However, recent phenotypic evidence suggests that immunogenetic variation, i.e. allelic variability in genes associated with the immune system, results in host-parasite genotype-by-genotype interactions and thus specific innate immune responses. Immunogenetic variation is common in all vertebrate taxa and this reflects an effective immunological function in complex environments. However, the underlying variability in host gene expression patterns as response of innate immunity to within-species genetic diversity of macroparasites in vertebrates is unknown. We hypothesized that intra-specific variation among parasite genotypes must be reflected in host gene expression patterns. Here we used high-throughput RNA-sequencing to examine the effect of parasite genotypes on gene expression patterns of a vertebrate host, the three-spined stickleback ( Gasterosteus aculeatus). By infecting naïve fish with distinct trematode genotypes of the species Diplostomum pseudospathaceum we show that gene activity of innate immunity in three-spined sticklebacks depended on the identity of an infecting macroparasite genotype. In addition to a suite of genes indicative for a general response against the trematode we also find parasite-strain specific gene expression, in particular in the complement system genes, despite similar infection rates of single clone treatments. The observed discrepancy between infection rates and gene expression indicates the presence of alternative pathways which execute similar functions. This suggests that the innate immune system can induce redundant responses specific to parasite genotypes.

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          Most cited references28

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          The genomic basis of adaptive evolution in threespine sticklebacks

          Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.
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            Innate immunity of fish (overview).

            The innate immune system is the only defence weapon of invertebrates and a fundamental defence mechanism of fish. The innate system also plays an instructive role in the acquired immune response and homeostasis and is therefore equally important in higher vertebrates. The innate system's recognition of non-self and danger signals is served by a limited number of germ-line encoded pattern recognition receptors/proteins, which recognise pathogen associated molecular patterns like bacterial and fungal glycoproteins and lipopolysaccharides and intracellular components released through injury or infection. The innate immune system is divided into physical barriers, cellular and humoral components. Humoral parameters include growth inhibitors, various lytic enzymes and components of the complement pathways, agglutinins and precipitins (opsonins, primarily lectins), natural antibodies, cytokines, chemokines and antibacterial peptides. Several external and internal factors can influence the activity of innate immune parameters. Temperature changes, handling and crowding stress can have suppressive effects on innate parameters, whereas several food additives and immunostimulants can enhance different innate factors. There is limited data available about the ontogenic development of the innate immunological system in fish. Active phagocytes, complement components and enzyme activity, like lysozyme and cathepsins, are present early in the development, before or soon after hatching.
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              The genome sequence of Atlantic cod reveals a unique immune system.

              Atlantic cod (Gadus morhua) is a large, cold-adapted teleost that sustains long-standing commercial fisheries and incipient aquaculture. Here we present the genome sequence of Atlantic cod, showing evidence for complex thermal adaptations in its haemoglobin gene cluster and an unusual immune architecture compared to other sequenced vertebrates. The genome assembly was obtained exclusively by 454 sequencing of shotgun and paired-end libraries, and automated annotation identified 22,154 genes. The major histocompatibility complex (MHC) II is a conserved feature of the adaptive immune system of jawed vertebrates, but we show that Atlantic cod has lost the genes for MHC II, CD4 and invariant chain (Ii) that are essential for the function of this pathway. Nevertheless, Atlantic cod is not exceptionally susceptible to disease under natural conditions. We find a highly expanded number of MHC I genes and a unique composition of its Toll-like receptor (TLR) families. This indicates how the Atlantic cod immune system has evolved compensatory mechanisms in both adaptive and innate immunity in the absence of MHC II. These observations affect fundamental assumptions about the evolution of the adaptive immune system and its components in vertebrates.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                25 September 2014
                : 9
                : 9
                : e108001
                Affiliations
                [1 ]Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany
                [2 ]Genetic Epidemiology of Vascular Disorders, Leibniz Institute for Arteriosclerosis Research at the University Münster, Münster, Germany
                [3 ]Institute for Evolution and Biodiversity, University of Münster, Münster, Germany
                [4 ]Department Evolutionary Ecology, Max-Planck Institute for Evolutionary Biology, Plön, Germany
                Chang Gung University, Taiwan
                Author notes

                Competing Interests: Monika Stoll is a PLOS ONE Editorial Board member. This does not alter the authors’ adherence to PLOS ONE Editorial policies and criteria.

                Conceived and designed the experiments: TBHR DH JKR MK. Performed the experiments: DH JKR MK. Analyzed the data: DH. Contributed reagents/materials/analysis tools: AW MS EBB. Wrote the paper: DH TBHR MK JKR EBB MS AW.

                Article
                PONE-D-14-19214
                10.1371/journal.pone.0108001
                4177871
                25254967
                bec2d851-566a-4c34-a6a7-0734f942766e
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 May 2014
                : 8 July 2014
                Page count
                Pages: 8
                Funding
                This study was financially supported by the Deutsche Forschungsgemeinschaft (DFG, Priority Programme SPP 1399 “Host-parasite Coevolution”; grant no. RE 1108/13-2 and RE 1108/13-1; dfg.de), GEOMAR Helmholtz Centre for Ocean Research Kiel ( www.geomar.de) and the Max Planck Institute for Evolutionary Biology ( www.evolbio.mpg.de). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Computational Biology
                Genome Analysis
                Transcriptome Analysis
                Genetics
                Gene Expression
                Genomics
                Immunology
                Immune System
                Innate Immune System
                Organisms
                Animals
                Invertebrates
                Flatworms
                Trematodes
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. Primary sequence is available at the NCBI sequence read archive (SRA) under the BioProject ID PRJNA253091.

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                Uncategorized

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