Dataset Information

Evolution of the IRF Family in Salmonids.

ABSTRACT: Interferon regulatory factors (IRFs) as a family, are major regulators of the innate antiviral response in vertebrates principally involved in regulating the expression of interferons (IFNs) and interferon-stimulated genes (ISGs). To date, nine IRFs have been identified in mammals with a 10th member also found in several avian and fish species. Through genome mining and phylogenetic analysis, we identified and characterised 23 irf genes in 6 salmonid species. This larger repertoire of IRF in salmonids results from two additional whole-genome duplications which occurred in early teleosts and salmonids, respectively. Synteny analysis was then used to identify and confirm which paralogues belonged to each subgroup and a new nomenclature was assigned to the salmonid IRFs. Furthermore, we present a full set of Real-Time PCR primers for all rainbow trout IRFs, confirmed by sequencing to ensure paralogue specificity. RT PCR was then used to examine the response of all trout irf genes in vivo, following Vibrio anguillarum and poly I:C stimulation, indicating potential functional divergence between paralogues. Overall, this study presents a comprehensive overview of the IRF family in salmonids and highlights some novel roles for the salmonid-specific IRFs in immunity.

SUBMITTER: Clark TC

PROVIDER: S-EPMC7915476 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Evolution of the IRF Family in Salmonids.

Clark Thomas C TC Boudinot Pierre P Collet Bertrand B

Genes 20210208 2

Interferon regulatory factors (IRFs) as a family, are major regulators of the innate antiviral response in vertebrates principally involved in regulating the expression of interferons (IFNs) and interferon-stimulated genes (ISGs). To date, nine IRFs have been identified in mammals with a 10th member also found in several avian and fish species. Through genome mining and phylogenetic analysis, we identified and characterised 23 <i>irf</i> genes in 6 salmonid species. This larger repertoire of IRF ...[more]

PMID: 33567584

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Project description:BackgroundSalmonids are of major importance both as farmed and wild animals. With the changing environment comes changes in pathogenic pressures so understanding the immune system of all salmonid species is of essence. Major histocompatibility complex (MHC) genes are key players in the adaptive immune system signalling infection to responding T-cells populations. Classical MHC class I (MHCI) genes, defined by high polymorphism, broad expression patterns and peptide binding ability, have a key role in inducing immunity. In salmonids, the fourth whole genome duplication that occurred 94 million years ago has provided salmonids with duplicate MHCI regions, while Northern Pike, a basal sister clade to salmonids, represent a species which has not experienced this whole genome duplication.ResultsComparing the gene organization and evolution of MHC class I gene sequences in Northern pike versus salmonids displays a complex picture of how many of these genes evolved. Regional salmonid Ia and Ib Z lineage gene duplicates are not orthologs to the Northern pike Z lineage sequences. Instead, salmonids have experienced unique gene duplications in both duplicate regions as well as in the Salmo and Oncorhynchus branch. Species-specific gene duplications are even more pronounced for some L lineage genes.ConclusionsAlthough both Northern pike as well as salmonids have expanded their U and Z lineage genes, these gene duplications occurred separately in pike and in salmonids. However, the similarity between these duplications suggest the transposable machinery was present in a common ancestor. The salmonid MHCIa and MHCIb regions were formed during the 94 MYA since the split from pike and before the Oncorhynchus and Salmo branch separated. As seen in tetrapods, the non-classical U lineage genes are diversified duplicates of their classical counterpart. One MHCI lineage, the L lineage, experienced massive species-specific gene duplications after Oncorhynchus and Salmo split approximately 25 MYA. Based on what we currently know about L lineage genes, this large variation in number of L lineage genes also signals a large functional diversity in salmonids.

Project description:BackgroundBATF family transcription factors (BATF, BATF2 and BATF3) form hetero-trimers with JUNB and either IRF4 or IRF8 to regulate cell fate in T cells and dendritic cells in vivo. While each combination of the hetero-trimer has a distinct role, some degree of cross-compensation was observed. The basis for the differential actions of IRF4 and IRF8 with BATF factors and JUNB is still unknown. We propose that the differences in function between these hetero-trimers may be caused by differences in their DNA binding preferences. While all three BATF family transcription factors have similar binding preferences when binding as a hetero-dimer with JUNB, the cooperative binding of IRF4 or IRF8 to the hetero-dimer/DNA complex could change the preferences. We used Spec-seq, which allows for the efficient and accurate determination of relative affinity to a large collection of sequences in parallel, to find differences between cooperative DNA binding of IRF4, IRF8 and BATF family members.ResultsWe found that without IRF binding, all three hetero-dimer pairs exhibit nearly the same binding preferences to both expected wildtype binding sites TRE (TGA(C/G)TCA) and CRE (TGACGTCA). IRF4 and IRF8 show the very similar DNA binding preferences when binding with any of the three hetero-dimers. No major change of binding preferences was found in the half-sites between different hetero-trimers. IRF proteins bind with substantially lower affinity with either a single nucleotide spacer between IRF and BATF binding site or with an alternative mode of binding in the opposite orientation. In addition, the preference to CRE binding site was reduced with either IRF binding in all BATF-JUNB combinations.ConclusionsThe specificities of BATF, BATF2 and BATF3 are all very similar as are their interactions with IRF4 and IRF8. IRF proteins binding adjacent to BATF sites increases affinity substantially compared to sequences with spacings between the sites, indicating cooperative binding through protein-protein interactions. The preference for the type of BATF binding site, TRE or CRE, is also altered when IRF proteins bind. These in vitro preferences aid in the understanding of in vivo binding activities.

Dataset Information

Evolution of the IRF Family in Salmonids.

Publications

Evolution of the IRF Family in Salmonids.

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