Biology subjects

Monsen, O.

Publications and source records attributed to Monsen, O..

4 recordsLinked to original sources

bioRxiv2024

The role of transposon activity in shaping cis-regulatory element evolution after whole genome duplication

Two of the most potent drivers of genome evolution in eukaryotes are whole genome duplications (WGD) and transposable element (TE) activity. These two mutational forces can also play synergistic roles; WGDs result in both cellular stress and functional redundancy, which would allow TEs to escape host-silencing mechanisms and effectively spread with reduced impact on fitness. As TEs can function as, or evolve into, TE-derived cis-regulatory elements (TE-CREs), bursts of TE-activity following WGD are likely to impact evolution of gene regulation. However, the role of TEs in genome regulatory remodelling after WGDs is unclear. Here we used the genome of Atlantic salmon, which is known to have experienced massive expansion of TEs after a WGD [~]100 Mya, as a model system to explore the synergistic roles of TEs and WGDs on genome regulatory evolution. We identified 55,080 putative TE-CREs in Atlantic salmon using chromatin accessibility data from brain and liver. Of these, 80% were tissue specific to liver (43%) or brain (37%) and TE-CREs originating from retroelements were twice as common as those originating from DNA elements. Signatures of selection shaping TE-CRE evolution were evident from depletion of TEs in open chromatin, a bias in tissue-shared TE-CREs towards older TE-insertions, as well as tissue-specific processes shaping the TE-CRE repertoire. A minority of TE-families (16%) accounted for the origin of 46% of all TE-CREs, but the transposition activity of these CRE-superspreader families happened mostly prior to the WGD. Analyses of individual TE-CREs do however support a significantly higher rate of TE-CRE evolution from insertions happening around the time of the salmonid WGD. This pattern was particularly striking for the DTT elements, despite having generally low propensity to evolve into TE-CREs and impact transcription. Furthermore, co-expression based analyses supported the presence of TE-driven gene regulatory network evolution, including DTT elements active at the time of WGD. In conclusion, we find a strong association between TE insertions at the time of WGD and TE-CRE evolution. This association was not driven by particular TE-families with high capability to evolve into TE-CREs but likely a consequence of the concurrent surge of novel TE insertions, mostly from DTT elements, in combination with a shift in selective pressure on genome regulation following the WGD.

evolutionary biology↗

bioRxiv2023

The genome regulatory landscape of Atlantic salmon liver through smoltification

The anadromous Atlantic salmon undergo a preparatory physiological transformation before seawater entry, referred to as smoltification. Key molecular developmental processes involved in this life stage transition, such as remodeling of gill functions, are known to be synchronized and modulated by environmental cues like photoperiod. However, little is known about the photoperiod influence and genome regulatory processes driving other canonical aspects of smoltification such as the large-scale changes in lipid metabolism and energy homeostasis in the developing smolt liver. Here we generate transcriptome, DNA methylation, and chromatin accessibility data from salmon livers across smoltification under different photoperiod regimes. We find a systematic reduction of expression levels of genes with a metabolic function, such as lipid metabolism, and increased expression of energy related genes such as oxidative phosphorylation, during smolt development in freshwater. However, in contrast to similar studies of the gill, smolt liver gene expression prior to seawater transfer was not impacted by photoperiodic history. Integrated analyses of gene expression and transcription factor (TF) binding signatures highlight likely important TF dynamics underlying smolt gene regulatory changes. We infer that ZNF682, KLFs, and NFY TFs are important in driving a liver metabolic shift from synthesis to break down of organic compounds in freshwater. Moreover, the increased expression of ribosomal associated genes after smolts were transferred to seawater was associated with increased occupancy of NFIX and JUN/FOS TFs proximal to transcription start sites, which could be the molecular consequence of rising levels of circulating growth hormones after seawater transition. We also identified differential methylation patterns across the genome, but associated genes were not functionally enriched or correlated to observed gene expression changes across smolt development. This contrasts with changes in TF binding which were highly correlated to gene expression, underscoring the relative importance of chromatin accessibility and transcription factor regulation in smoltification. Author summaryAtlantic salmon migrate between freshwater and seawater as they mature and grow. To survive the transition between these distinct environments, salmon transform their behavior, morphology, and physiology through the process of smoltification. One important adaptation to life at sea is remodeling of metabolism in the liver. It is unknown, however, whether this is a preadaptation that occurs before migration, what degree this is influenced by day length like other aspects of smoltification, and how gene regulatory programs shift to accomplish this transformation. We addressed these questions through a time course experiment where salmon were exposed to short and long day lengths, smoltified, and transferred to seawater. We sampled the livers and measured changes in gene expression, DNA methylation, chromatin accessibility, and transcription factor binding. We found metabolic remodeling occurred in freshwater before exposure to seawater and that day length did not have any long-term effects in liver. Transcription factor binding dynamics were closely linked to gene expression changes, and we describe transcription factors with key roles in smoltification. In stark contrast, we found no links between gene expression changes and DNA methylation patterns. This work deepens our understanding of the regulatory gear shifts associated with metabolic remodeling during smoltification.

genomics↗

bioRxiv2022

Functional validation of transposable element derived cis-regulatory elements in Atlantic salmon

BackgroundTransposable elements (TEs) are hypothesized to play important roles in shaping genome evolution following whole genome duplications (WGD), including rewiring of gene regulation. In a recent analysis, duplicate gene copies that had evolved higher expression in liver following the salmonid WGD ~100 million years ago were associated with higher numbers of predicted TE-derived cis-regulatory elements (TE-CREs). Yet, the ability of these TE-CREs to recruit transcription factors (TFs) in vivo and impact gene expression remains unknown. ResultsHere, we evaluated the gene regulatory functions of 11 TEs using luciferase promoter reporter assays in Atlantic salmon (Salmo salar) primary liver cells. Canonical Tc1-Mariner elements from intronic regions showed no or small repressive effects on transcription. However, other TE-derived cis-regulatory elements upstream of transcriptional start sites increased expression significantly. ConclusionOur results question the hypothesis that TEs in the Tc1-Mariner superfamily, which were extremely active following WGD in salmonids, had a major impact on regulatory rewiring of gene duplicates, but highlights the potential of other TEs in post-WGD rewiring of gene regulation in the Atlantic salmon genome.

evolutionary biology↗

bioRxiv2020

Comparative regulomics reveals pervasive selection on gene dosage following whole genome duplication

Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80-100 million years ago. We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Although ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards pseudogenization, strong evolutionary constraints have frequently also favoured symmetric shifts in gene dosage of both copies, likely to achieve gene dose reduction while avoiding accumulation of toxic mutations. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one source of novel binding sites driving tissue-specific gains in expression. Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.

evolutionary biology↗