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Torresen, O. K.

Publications and source records attributed to Torresen, O. K..

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Evolutionary adaptability linked to length variation in short genic tandem repeats

Intrinsically disordered protein regions are of high importance for temperature sensing and immune responses in plants. Tracts of identical amino acids accumulate in these regions and can vary in length over generations due to expansions and retractions of short tandem repeats at the genomic level. However, little attention has been paid to what extent length variation is shaped by natural selection. By environmental association analysis on 2,514 length variable tracts in 770 whole-genome sequenced wild Arabidopsis thaliana we show that length variation in glutamine and asparagine amino acid homopolymers, as well as in interaction hotspots, correlate with local bio-climatic habitat. We determined experimentally that the promoter activity of a light-stress gene depended on polyglutamine length variants in a disordered transcription factor. Our results show that length variations impact protein function and are substantially shaped by natural selection. Length variants modulating protein function at a global genomic scale has implications for understanding protein evolution and eco-evolutionary biology.

evolutionary biology

Long-read sequence capture elucidates the evolution of the hemoglobin gene clusters in codfishes

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 hemoglobin (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 (~100kb) and MN (~200kb) clusters, which include syntenic regions of coding and intergenic sequences. Our results revealed an overall conserved genetic organization and synteny 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.

genomics

Genomic architecture of codfishes featured by expansions of innate immune genes and short tandem repeats

BackgroundIncreased availability of genome assemblies for non-model organisms has resulted in invaluable biological and genomic insight into numerous vertebrates including teleosts. The sequencing and assembly of the Atlantic cod (Gadus morhua) genome and the genomes of many of its relatives (Gadiformes) demonstrated a shared loss 100 million years ago of the major histocompatibility complex (MHC) II genes. The recent publication of an improved version of the Atlantic cod genome assembly reported an extreme density of tandem repeats compared to other vertebrate genome assemblies. Highly contiguous genome assemblies are needed to further investigate the unusual immune system of the Gadiformes, and the high density of tandem repeats in this group.\n\nResultsHere, we have sequenced and assembled the genome of haddock (Melanogrammus aeglefinus) - a relative of Atlantic cod - using a combination of PacBio and Illumina reads. Comparative analyses uncover that the haddock genome contains an even higher density of tandem repeats outside and within protein coding sequences than Atlantic cod. Further, both species show an elevated number of tandem repeats in genes mainly involved in signal transduction compared to other teleosts. An in-depth characterization of the immune gene repertoire demonstrates a substantial expansion of MCHI in Atlantic cod compared to haddock. In contrast, the Toll-like receptors show a similar pattern of gene losses and expansions. For another gene family associated with the innate immune system, the NOD-like receptors (NLRs), we find a large expansion common to all teleosts, with possible lineage-specific expansions in zebrafish, stickleback and the codfishes.\n\nConclusionsThe generation of a highly contiguous genome assembly of haddock revealed that the high density of short tandem repeats as well as expanded immune gene families is not unique to Atlantic cod - but most likely a feature common to all codfishes. A shared expansion of NLR genes in teleosts suggests that the NLRs have a more substantial role in the innate immunity of teleosts than other vertebrates. Moreover, we find that high copy number genes combined with variable genome assembly qualities may impede complete characterization, i.e. the number of NLRs might be underestimates in the different teleost species.

genomics

The most developmentally truncated fishes show extensive Hox gene loss and miniaturized genomes

Hox genes play a fundamental role in regulating the embryonic development of all animals. Manipulation of these transcription factors in model organisms has unraveled key aspects of evolution, like the transition from fin to limb. However, by virtue of their fundamental role and pleiotropic effects, simultaneous knockouts of several of these genes pose significant challenges. Here, we report on evolutionary simplification in two species of the dwarf minnow genus Paedocypris using whole genome sequencing. The two species feature unprecedented Hox gene loss and genome reduction in association with their massive developmental truncation. We also show how other genes involved in the development of musculature, nervous system, and skeleton have been lost in Paedocypris, mirroring its highly progenetic phenotype. Further, we identify two mechanisms responsible for genome streamlining: severe intron shortening and reduced repeat content. As a naturally simplified system closely related to zebrafish, Paedocypris provides novel insights into vertebrate development.

genomics

The grayling genome reveals selection on gene expression regulation after whole genome duplication

Whole genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ~80 million years ago (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to investigate the evolutionary consequences of WGD. Here, we present a draft genome assembly of European grayling (Thymallus thymallus) and use this in a comparative framework to study evolution of gene regulation following WGD. Among the Ss4R duplicates identified in European grayling and Atlantic salmon (Salmo salar), one third reflect non-neutral tissue expression evolution, with strong purifying selection, maintained over ~50 million years. Of these, the majority reflect conserved tissue regulation under strong selective constraints related to brain and neural-related functions, as well as higher-order protein-protein interactions. A small subset of the duplicates has evolved tissue regulatory expression divergence in a common ancestor, which have been subsequently conserved in both lineages, suggestive of adaptive divergence following WGD. These candidates for adaptive tissue expression divergence have elevated rates of protein coding- and promoter-sequence evolution and are enriched for immune- and lipid metabolism ontology terms. Lastly, lineage-specific duplicate divergence points towards underlying differences in adaptive pressures on expression regulation in the non-anadromous grayling versus the anadromous Atlantic salmon.\n\nOur findings enhance our understanding of the role of WGD in genome evolution and highlights cases of regulatory divergence of Ss4R duplicates, possibly related to a niche shift in early salmonid evolution.

genomics