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The whole-genome duplication 80 million years ago of the common ancestor of salmonids (salmonid-specific fourth vertebrate whole-genome duplication, Ss4R) provides unique opportunities to learn about the evolutionary fate of a duplicated vertebrate genome in 70 extant lineages. Here we present a high-quality genome assembly for Atlantic salmon ( Salmo salar ), and show that large genomic reorganizations, coinciding with bursts of transposon-mediated repeat expansions, were crucial for the post-Ss4R rediploidization process. Comparisons of duplicate gene expression patterns across a wide range of tissues with orthologous genes from a pre-Ss4R outgroup unexpectedly demonstrate far more instances of neofunctionalization than subfunctionalization. Surprisingly, we find that genes that were retained as duplicates after the teleost-specific whole-genome duplication 320 million years ago were not more likely to be retained after the Ss4R, and that the duplicate retention was not influenced to a great extent by the nature of the predicted protein interactions of the gene products. Finally, we demonstrate that the Atlantic salmon assembly can serve as a reference sequence for the study of other salmonids for a range of purposes. The genome sequence is presented for the Atlantic salmon (Salmo salar), providing information about a rediploidization following a salmonid-specific whole-genome duplication event that resulted in an autotetraploidization. A window on salmonid genome evolution William Davidson and colleagues report sequencing and assembly of the Atlantic salmon genome, which they demonstrate as a useful reference to also improve the genome assembly of other salmanoids. Their analyses provide insights into duplicate retention patterns across two rounds of whole-genome duplication that have occurred in this lineage.

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, chromatin accessibility, and transcription factor (TF) binding signatures highlight chromatin remodeling and TF dynamics underlying smolt gene regulatory changes. Differential peak accessibility patterns largely matched differential gene expression patterns during smoltification and 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. Overall, chromatin accessibility and TFBS occupancy were highly correlated to changes in gene expression. On the other hand, we identified numerous differential methylation patterns across the genome, but associated genes were not functionally enriched or correlated to observed gene expression changes across smolt development. Taken together, this work highlights the relative importance of chromatin remodeling during smoltification and demonstrates that metabolic remodeling occurs as a preadaptation to life at sea that is not to a large extent driven by photoperiod history.

To ensure sustainable aquaculture, it is essential to understand the path ‘from feed to fish’, whereby the gut microbiome plays an important role in digestion and metabolism, ultimately influencing host health and growth. Previous work has reported the taxonomic composition of the Atlantic salmon (Salmo salar) gut microbiome; however, functional insights are lacking. Here we present the Salmon Microbial Genome Atlas consisting of 211 high-quality bacterial genomes, recovered by cultivation (n = 131) and gut metagenomics (n = 80) from wild and farmed fish both in freshwater and seawater. Bacterial genomes were taxonomically assigned to 14 different orders, including 35 distinctive genera and 29 previously undescribed species. Using metatranscriptomics, we functionally characterized key bacterial populations, across five phyla, in the salmon gut. This included the ability to degrade diet-derived fibres and release vitamins and other exometabolites with known beneficial effects, which was supported by genome-scale metabolic modelling and in vitro cultivation of selected bacterial species coupled with untargeted metabolomic studies. Together, the Salmon Microbial Genome Atlas provides a genomic and functional resource to enable future studies on salmon nutrition and health.

The gastrointestinal microbiota plays a pivotal role in shaping host physiology and health. By selectively promoting bacteria associated with improved host health, microbiota-directed fibres offer a strategy to enhance the beneficial functions of the microbiota. In this work, we developed a pH-controlled in vitro fermentation system (InVitSim) as a model to evaluate the effects of such a fibre – acetylated galactoglucomannan from Norway spruce – on the composition and functionality of porcine caecal microbial communities. We validated the experimental outcomes by comparing the response of the in vitro model to a previous in vivo feeding trial utilising the same β-mannan fibres. Long-read sequencing with Oxford Nanopore, metatranscriptomics, and short-chain fatty acid measurements were undertaken to survey microbial community dynamics and functionality. Microbial communities in pigs and InVitSim responded similarly to β-mannan supplementation, with taxa like Prevotella, Catenibacterium, and Faecalibacterium increasing in abundance. Intriguingly, some taxa were observed to be more affected by β-mannan supplementation in InVitSim than in vivo. These taxa included several bacterial species that were not previously known to utilise β-mannan, yet exhibited upregulated genes encoding carbohydrate-active enzymes involved in the degradation of this substrate.

Risk assessment and protection of plant communities in contaminated ecosystems require in-depth understanding of differential sensitivity to chronic ionising radiation in plants. However, the contributing molecular factors to differential radiosensitivity among plant species are poorly understood. To shed light on this, we compared early events associated with protection, repair, and stress responses in gamma-irradiated (1-290 mGy h−1) seedlings of the radiosensitive conifer Norway spruce (Picea abies) and the radiotolerant Arabidopsis thaliana, by analysing growth, organelle and DNA damage, transcriptomes and the dynamics of antioxidant activities and expression of relevant genes. After 48 h of gamma radiation exposure, Norway spruce showed significantly reduced growth at 100-290 mGy h−1 and organelle damage, especially in mitochondria, at ≥ 1 mGy h−1 whereas A. thaliana showed normal vegetative growth at all dose rates, transiently delayed reproductive development at 290 mGy h−1 only, minor organelle damage only at ≥ 100 mGy h−1 and significantly less DNA damage than in Norway spruce at all dose rates. Comparative transcriptomics revealed that A. thaliana showed massive activation of genes related to DNA damage repair, antioxidants, and other stress responses at ≥ 1 mGy h−1 while Norway spruce mobilized transcription of such pathways only at ≥ 40 mGy h−1. The transcriptional activation of repair and protection responses at higher gamma dose-rates only and its absence in lower dose-rates, correlates with high radiosensitivity of Norway spruce, compared to the massive transcriptional activation from low dose-rates in the radiotolerant A. thaliana.

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.Competing Interest StatementThe authors have declared no competing interest.Footnotes* We have implemented a new method to identify TEs enriched in open chromatin that takes genomic context into account. We reran all our analyses with improved TE-divergence estimates (CpG normalised Kimura divergence) When implementing the use of Kimura distances instead of %-divergence we also had to come up with a new and empirically derived cutoff for how to define TE-activity relative to the WGD. We have added a new analysis of temporal co-occurrence between TE-CREs and WGD (Figures 4 G-H) which revealed patterns we overlooked in the first version. We have revised the text to address confusions and lack of clarity in some parts of the manuscript. The implementation of the new enrichment tests did not change the overall results. Neither did the use of Kimura distances and the new approach to classify temporal activity relative to the WGD for entire TE-families. However, our new analysis that take the full heterogeneity of TE-CRE ages into account did support a strong enrichment of TE-CREs originating from the time around the WGD.

Little is known about the evolution of cold tolerance in polar plant species and how they differ from their temperate relatives. To gain insight into their biology and the evolution of cold tolerance, we compared the molecular basis of cold response in three Arctic Brassicaceae species. We conducted a comparative time series experiment to examine transcriptional responses to low temperature. RNA was sampled at 22 degrees Celsius, and after 3h, 6h, and 24h at 2 degrees Celsius. We then identified sets of genes that were differentially expressed in response to cold and compared them between species, as well as to published data from the temperate Arabidopsis thaliana. Most differentially expressed genes were species-specific, but a significant portion of the cold response was also shared among species. Among thousands of differentially expressed genes, ~200 were shared among the three Arctic species and A. thaliana, while ~100 were exclusively shared among the three Arctic species. Our results show that cold response differs markedly between Arctic Brassicaceae species, but likely builds on a conserved basis found across the family. They also confirm that highly polygenic traits such as cold tolerance may show little repeatability in their patterns of adaptation. Competing Interest Statement The authors have declared no competing interest. Footnotes * Updated Blast and topGO results. Added comparison of co-expression modules. Some figures and tables moved to Supplementary.

Research conducted: The phytohormone ethylene impacts secondary stem growth in plants by stimulating cambial activity, xylem development and fiber over vessel formation. Here we report the effect of ethylene on secondary cell wall formation and the molecular connection between ethylene signaling and wood formation. Methods: We applied exogenous ethylene or its precursor 1-aminocyclopropane-1-carboxylic acid (ACC) to wild type and ethylene insensitive hybrid aspen trees (Populus tremula x tremuloides) and studied secondary cell wall anatomy, chemistry and ultrastructure. We furthermore analyzed the transcriptome (RNA Seq) after ACC application to wild type and ethylene insensitive trees. Key results: We demonstrate that ACC and ethylene induce gelatinous-layers (G-layers) and alter the fiber cell wall cellulose microfibril angle. G-layers are tertiary wall layers rich in cellulose, typically found in tension wood of aspen trees. A vast majority of transcripts affected by ACC are downstream of ethylene perception and include a large number of transcription factors (TFs). Motif-analyses reveal potential connections between ethylene TFs (ERFs, EIN3/EIL1) and wood formation. Conclusion: G-layer formation upon ethylene application suggests that the increase in ethylene biosynthesis observed during tension wood formation is important for its formation. Ethylene-regulated TFs of the ERF and EIN3/EIL1 type could transmit the ethylene signal.