Genomic architecture of haddock (Melanogrammus aeglefinus) shows expansions of innate immune genes and short tandem repeats

Tørresen, Ole K.; Brieuc, Marine S. O.; Solbakken, Monica Hongrø; Sørhus, Elin; Nederbragt, Alexander Johan; Jakobsen, Kjetill S.; Meier, Sonnich; Edvardsen, Rolf B.; Jentoft, Sissel

doi:10.1186/s12864-018-4616-y

Cited by 45 publications

(53 citation statements)

References 112 publications

(164 reference statements)

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“…Organization of the Hb gene clusters. At the top, the reconstructed micro‐synteny of the haemoglobin gene clusters is shown based on the genomes of Atlantic cod (Tørresen et al., ; gadMor2) and haddock (Tørresen et al., ; melAeg). Below, we illustrate the genomic synteny inferred from the de novo assemblies for the eight species included in the capture experiment, mapped on a time‐calibrated species phylogeny modified from Malmstrøm et al.…”

Section: Resultsmentioning

confidence: 99%

Long‐read sequence capture of the haemoglobin gene clusters across codfish species

Hoff

Baalsrud

Tooming‐Klunderud

et al. 2018

Molecular Ecology Resources

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Combining high-throughput sequencing with targeted sequence capture has become an attractive tool to study specific genomic regions of interest. Most studies have so far focused on the exome using short-read technology. These approaches are not designed to capture intergenic regions needed to reconstruct genomic organization, including regulatory regions and gene synteny. Here, we demonstrate the power of combining targeted sequence capture with long-read sequencing technology for comparative genomic analyses of the haemoglobin (Hb) gene clusters across eight species separated by up to 70 million years. Guided by the reference genome assembly of the Atlantic cod (Gadus morhua) together with genome information from draft assemblies of selected codfishes, we designed probes covering the two Hb gene clusters. Use of custom-made barcodes combined with PacBio RSII sequencing led to highly continuous assemblies of the LA (~100 kb) and MN (~200 kb) clusters, which include syntenic regions of coding and intergenic sequences. Our results revealed an overall conserved genomic organization of the Hb genes within this lineage, yet with several, lineage-specific gene duplications.Moreover, for some of the species examined, we identified amino acid substitutions at two sites in the Hbb1 gene as well as length polymorphisms in its regulatory region, which has previously been linked to temperature adaptation in Atlantic cod populations. This study highlights the use of targeted long-read capture as a versatile approach for comparative genomic studies by generation of a cross-species genomic resource elucidating the evolutionary history of the Hb gene family across the highly divergent group of codfishes. K E Y W O R D Scodfishes, comparative genomics, Gadiformes, PacBio sequencing, targeted sequence capture, teleosts *These authors contributed equally to this work.---

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Section: Resultsmentioning

confidence: 99%

Long‐read sequence capture of the haemoglobin gene clusters across codfish species

Hoff

Baalsrud

Tooming‐Klunderud

et al. 2018

Molecular Ecology Resources

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“…For the second pass, SNAP and AUGUSTUS were retrained with the generated MAKER2 predictions and otherwise performed with the same setup. The resulting gene predictions had domain annotations and putative functions added using InterProScan v5.4.47 and BLASTp against the UniProt database with evalue 1e-5 (same methodology as [86,88]). Finally, the output was filtered using the MAKER2 default filtering approach only retaining predictions with AED <1.…”

Section: Methodsmentioning

confidence: 99%

The genome of the plague-resistant great gerbil reveals species-specific duplication of an MHCII gene

Nilsson

Schmid

et al. 2018

Preprint

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Background The great gerbil (Rhombomys opimus) is a social rodent living in permanent, complex burrow systems distributed throughout Central Asia, where it serves as the main host of several important vector-borne infectious diseases and is defined as a key reservoir species for plague (Yersinia pestis). Studies from the wild have shown that the great gerbil is largely resistant to plague but the genetic basis for resistance is yet to be determined. Results Here, we present a highly contiguous annotated genome assembly of great gerbil, covering over 96 % of the estimated 2.47 Gb genome. Comparative genomic analyses focusing on the immune gene repertoire, reveal shared gene losses within TLR gene families (i.e. TLR8, TLR10 and all members of TLR11-subfamily) for the Gerbillinae lineage, accompanied with signs of diversifying selection of TLR7 and TLR9. Most notably, we find a great gerbil-specific duplication of the MHCII DRB locus. In silico analyses suggest that the duplicated gene provides high peptide binding affinity for Yersiniae epitopes. Conclusion The great gerbil genome provides new insights into the genomic landscape that confers immunological resistance towards plague. The high affinity for Yersinia epitopes could be key in our understanding of the high resistance in great gerbils, putatively conferring a faster initiation of the adaptive immune response leading to survival of the infection. Our study demonstrates the power of studying zoonosis in natural hosts through the generation of a genome resource for further comparative and experimental work on plague survival and evolution of host-pathogen interactions.

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“…NLRs have diverse roles from direct pathogen recognition to transcriptional regulation of the MHC (NLRs CIITA and NLRC5) and contribute to inflammasome activation [100]. Mammalian genomes display 20-40 NLRs in families NLR-A and NLR-B, while fish also feature a fish-specific subfamily (NLR-C) [101] and a much expanded NLR repertoire (e.g., 405 NLR-C genes in zebrafish, Danio rerio) [102,103]. Other species in which the Table S8 for annotation details), which include 9 highly conserved vertebrate NLRs (NOD1, NOD2, NLRC3, NLRC5, NLRX1, NWD1, NWD2, APAF1, CIITA) as well as 344 NLR-C genes.…”

Section: Response To the Environment: Immune Systemmentioning

confidence: 99%

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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Genomic architecture of haddock (Melanogrammus aeglefinus) shows expansions of innate immune genes and short tandem repeats

Cited by 45 publications

References 112 publications

Long‐read sequence capture of the haemoglobin gene clusters across codfish species

Long‐read sequence capture of the haemoglobin gene clusters across codfish species

The genome of the plague-resistant great gerbil reveals species-specific duplication of an MHCII gene

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

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