Alternative haplotypes of antigen processing genes in zebrafish diverged early in vertebrate evolution

McConnell, Sean C.; Hernandez, Kyle M.; Wcisel, Dustin J.; Kettleborough, Ross; Stemple, Derek L.; Yoder, Jeffrey A.; Andrade, Jorge; Jong, Jill L. O. de

doi:10.1073/pnas.1607602113

Cited by 51 publications

(73 citation statements)

References 84 publications

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“…The round goby has two copies of TAP2, which promotes the delivery of peptides to MHCI (annotated as TAP2 and TAP2T; see Additional file 14: Figure S8 for a phylogenetic tree of TAP genes). Two TAP2 genes have also been described in zebrafish (Danio rerio), and our results thus suggest this is a conserved feature among teleosts [92]. In addition, we identify the MHC transcriptional regulators CIITA and NLRC5.…”

Section: Response To the Environment: Immune Systemsupporting

confidence: 62%

The round goby genome provides insights into mechanisms that may facilitate biological invasions

et al. 2020

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Background: The invasive benthic round goby (Neogobius melanostomus) is the most successful temperate invasive fish and has spread in aquatic ecosystems on both sides of the Atlantic. Invasive species constitute powerful in situ experimental systems to study fast adaptation and directional selection on short ecological timescales and present promising case studies to understand factors involved the impressive ability of some species to colonize novel environments. We seize the unique opportunity presented by the round goby invasion to study genomic substrates potentially involved in colonization success. Results: We report a highly contiguous long-read-based genome and analyze gene families that we hypothesize to relate to the ability of these fish to deal with novel environments. The analyses provide novel insights from the large evolutionary scale to the small species-specific scale. We describe expansions in specific cytochrome P450 enzymes, a remarkably diverse innate immune system, an ancient duplication in red light vision accompanied by red skin fluorescence, evolutionary patterns of epigenetic regulators, and the presence of osmoregulatory genes that may have contributed to the round goby's capacity to invade cold and salty waters. A recurring theme across all analyzed gene families is gene expansions. Conclusions: The expanded innate immune system of round goby may potentially contribute to its ability to colonize novel areas. Since other gene families also feature copy number expansions in the round goby, and since other Gobiidae also feature fascinating environmental adaptations and are excellent colonizers, further long-read genome approaches across the goby family may reveal whether gene copy number expansions are more generally related to the ability to conquer new habitats in Gobiidae or in fish.

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Section: Response To the Environment: Immune Systemsupporting

confidence: 62%

The round goby genome provides insights into mechanisms that may facilitate biological invasions

et al. 2020

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“…Although NK cells clearly exist in ectotherms, identification of NKRs has been exceedingly difficult owing to the rapid evolution of this system 20 ; nevertheless, NKR genes, which are linked to the MHC, have been found in all vertebrates, demonstrating an early (likely primordial) association of MHC class I and NKRs 21,22 . Ancient lineages of genes encoding MHC class I molecules, immunoproteasome and transporter associated with antigen processing (TAP) molecules are found in the MHC of all fish and amphibians studied so far, but in mammals, this prototype has been superseded by a system that is less rigid in MHC class I peptide specificity 21,23–25 . A large leap forward in evolution is clear in amphibians, which show canonical antibody class switching and have an IgG class (known as IgY) that is involved in typical memory immune responses 26 (FIG.…”

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confidence: 99%

A cold-blooded view of adaptive immunity

2018

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The adaptive immune system arose 500 million years ago in ectothermic (cold-blooded) vertebrates. Classically, the adaptive immune system has been defined by the presence of lymphocytes expressing recombination-activating gene (RAG)-dependent antigen receptors and the MHC. These features are found in all jawed vertebrates, including cartilaginous and bony fish, amphibians and reptiles and are most likely also found in the oldest class of jawed vertebrates, the extinct placoderms. However, with the discovery of an adaptive immune system in jawless fish based on an entirely different set of antigen receptors — the variable lymphocyte receptors — the divergence of T and B cells, and perhaps innate-like lymphocytes, goes back to the origin of all vertebrates. This Review explores how recent developments in comparative immunology have furthered our understanding of the origins and function of the adaptive immune system.

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“…This comprises some genes whose evolutionary history is extremely difficult to trace due to multiple copies and extensive polymorphism, such as MHC class I genes. Here, only mhc1zba was found to be a zebrafish ISG, but this does not necessarily imply that other zebrafish MHC class I genes are not ISGs, as they may have been missed due to mapping issues; the strain we used (AB) is not the same as the one of the reference genome (Tü), and strain-specific divergences are considerable between strains for MHC class I, with deep evolutionary roots (44). Importantly, we did not define ancestral ISGs for zebrafish-human ISG pairs that appeared to be related at first glance, but, upon further analysis, were too distant; for example, zebrafish vamp5 and human VAMP8 are both ISGs, but share their last common ancestor at the Opistokontha level, before the split of fungi and animals, very long before the emergence of IFNs.…”

Section: Discussionmentioning

confidence: 92%

Interferon-stimulated genes in zebrafish and human define an ancient arsenal of antiviral immunity

Levraud

Jouneau

Briolat

et al. 2019

Preprint

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The evolution of the interferon (IFN) system, the major innate antiviral mechanism of vertebrates, remains poorly understood. According to the detection of type I IFN genes in cartilaginous fish genomes, the system appeared 500My ago. However, the IFN system integrates many other components, most of which are encoded by IFN-stimulated genes (ISGs). To shed light on its evolution, we have used deep RNA sequencing to generate a comprehensive list of ISGs of zebrafish, taking advantage of the high quality genome annotation in this species. We analyzed larvae after inoculation of recombinant zebrafish type I IFN, or infection with chikungunya virus, a potent IFN inducer. We identified more than 400 zebrafish ISGs, defined as being either directly induced by IFN or induced by the virus in an IFN receptor-dependent manner. Their human orthologues were highly enriched in ISGs, particularly for highly-inducible genes. We identified 72 orthology groups containing ISGs in both zebrafish and human, revealing a core ancestral ISG repertoire, which includes most of the known signaling components of the IFN system. Many downstream effectors were also already present 450 My ago in the common ancestor of tetrapods and bony fish, and diversified as multi-gene families independently in the two lineages. A large proportion of the ISG repertoire is lineage-specific; around 40% of protein-coding zebrafish ISGs had no human orthologue. We identified 14 fish-specific gene families containing multiple ISGs, including finTRIMs. This work illuminates the evolution of the IFN system and provides a rich resource to explore new antiviral mechanisms.Key pointsWe established an exhaustive list of larval zebrafish ISGs.Orthologous ISGs in fish and human identify a large ancestral ISG repertoire.

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Alternative haplotypes of antigen processing genes in zebrafish diverged early in vertebrate evolution

Cited by 51 publications

References 84 publications

The round goby genome provides insights into mechanisms that may facilitate biological invasions

The round goby genome provides insights into mechanisms that may facilitate biological invasions

A cold-blooded view of adaptive immunity

Interferon-stimulated genes in zebrafish and human define an ancient arsenal of antiviral immunity

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