Alternative splicing in seasonal plasticity and the potential for adaptation to environmental change

Steward, Rachel; Jong, Maaike de; Oostra, Vicencio; Wheat, Christopher W.

doi:10.1038/s41467-022-28306-8

Cited by 41 publications

(40 citation statements)

References 93 publications

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“…Increasing temperatures induced alteration in the abundance of transcripts associated with post‐transcriptional modifications in both populations of lake sturgeon, influencing cellular plasticity. Conserved responses of alternative splicing and gene silencing via miRNA suggest that these mechanisms are part of the inducible stress response of sturgeons and likely play a role in regulating phenotypic plasticity, as observed in other fishes (Healy & Schulte, 2019; Shiina & Shimizu, 2020; Somero, 2018; Steward et al, 2022; Tan, Wang, Tian, Niu, Zhou, Jin, et al, 2019; Tan, Wang, Tian, Niu, Zhou, Yang, et al, 2019; Thorstensen, Turko, et al, 2022; Verta & Jacobs, 2021). However, these processes were ultimately downregulated as temperatures increased to 24°C, indicating thermal thresholds on post‐translational as well as transcriptional responsiveness.…”

Section: Discussionmentioning

confidence: 89%

Elevated temperatures reduce population‐specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

et al. 2023

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Rising mean and variance in temperatures elevates threats to endangered freshwater species such as lake sturgeon, Acipenser fulvescens. Previous research demonstrated that higher temperatures during development result in physiological consequences for lake sturgeon populations throughout Manitoba, Canada, with alteration of metabolic rate, thermal tolerance, transcriptional responses, growth and mortality. We acclimated lake sturgeon (30-60 days post fertilization, a period of high mortality) from northern and southern populations (56°02′46.5″N, 96°54′18.6″W and 50°17′52″N, 95°32′51″W, respectively, separated by approximately 650 km) within Manitoba to current (summer highs of 20-23°C) and future projected (+2-3°C) environmental temperatures of 16, 20 and 24°C for 30 days, and we measured gill transcriptional responses using RNAseq. Transcripts revealed SNPs consistent with genetically distinct populations and transcriptional responses altered by acclimation temperature. There were a higher number of differentially expressed transcripts observed in the southern, compared to the northern, population as temperatures increased, indicating enhanced transcriptional plasticity. Both lake sturgeon populations responded to elevated acclimation temperatures by downregulating the transcription of genes involved in protein synthesis and energy production. Furthermore, there were population-specific thresholds for the downregulation of processes promoting transcriptional plasticity as well as mitochondrial function as the northern population showed decreases at 20°C, while this capacity was not diminished until 24°C in the southern population. These transcriptional responses highlight the molecular impacts of increasing temperatures for divergent lake sturgeon populations during vulnerable developmental periods and the critical influence of transcriptome plasticity on acclimation capacity.

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Section: Discussionmentioning

confidence: 89%

Elevated temperatures reduce population‐specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

et al. 2023

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“…Increasing temperatures induced upregulation of transcripts associated with posttranscriptional modifications in both populations of lake sturgeon, enhancing translational plasticity. Conserved responses of alternative splicing and gene silencing via miRNA suggest that these mechanisms are part of the inducible stress response of sturgeons, similar to other studied fishes, and likely play a role in environmental adaptation (Somero, 2018;Healy & Schulte, 2019;Tan et al, 2019;Shiina and Shimizu, 2020;Verta and Jacobs, 2021;Thorstensen et al, 2022;Steward et al, 2022). However, these processes were ultimately downregulated as temperatures increased to 24 °C, indicating thermal thresholds on post-translational as well as transcriptional responsiveness.…”

Section: Plasticity As An Adaptive Traitmentioning

confidence: 90%

“…Histone level methylation ( carm1 ) alters the structure and availability of DNA for transcription, promoting phenotypic modification at the DNA level, allowing lake sturgeon to rapidly respond to environmental change (Burggren and Crews, 2014). Additionally, post-transcriptional modifications by pre-mRNA splicing ( larp7 ; Frilander and Barboric, 2020) can provide enhanced transcriptional plasticity, with the potential for enhanced adaptation to environmental change (Steward et al, 2022). Together, these two processes enhance the ability of lake sturgeon to modify the production of mRNAs prior to translation, and likely promote phenotypic plasticity towards increasing temperatures.…”

Section: Discussionmentioning

confidence: 99%

Elevated temperatures reduce population-specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Bugg

Thorstensen

Marshall

et al. 2022

Preprint

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Rising mean and variance in temperatures elevate threats to endangered freshwater species like the lake sturgeon, Acipenser fulvescens. Previous research has demonstrated that higher temperatures in early development result in physiological consequences for lake sturgeon populations throughout Manitoba, Canada, with alteration of metabolic rate, thermal tolerance, transcriptional responses, growth, and mortality. In the present study, we acclimated lake sturgeon from northern and southern populations within Manitoba to current and future projected environmental temperatures of 16, 20, and 24C for 30 days, and measured gill transcriptional responses using RNAseq. We found population-specific and acclimation-specific responses to the thermal treatments, as well as conserved molecular responses between northern and southern sturgeon populations. Expression profiles revealed a gradient in transcriptional responses consistent with acclimation temperature, with a higher number of differentially expressed transcripts observed in the southern compared to the northern lake sturgeon population as temperatures increase, indicating enhanced transcriptional plasticity. Overall lake sturgeon populations responded to thermal acclimation by upregulating the expression of transcripts involved in transcriptional and translational regulation, mitochondrial function, pathogen responses, and DNA damage, as well as genes associated with pre- and post-transcriptional processes (i.e., methylation, alternative splicing). Further, both populations upregulated transcript expression related to cell structural damage as temperatures increased to 20C, but the northern population also responded with increases in damage signaling and recruitment of mitochondrial processes involved in ATP production. Ultimately, these transcriptional responses highlight molecular consequences of increasing temperatures for divergent lake sturgeon populations during vulnerable early developmental periods and the critical influence of transcriptome plasticity on acclimation capacity.

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“…It remains unclear just how pervasive MH is in different types of biological sequence data, although our current and previous results (Lucaci et al ., 2021), and other studies (Cohen et al ., 2021; Freitas and Nery, 2022; Hensley et al ., 2021; MacLean et al ., 2021; Steward et al ., 2022) suggest that MH occurs broadly over diverse taxonomic groups. We expect that future research with interdisciplinary design combining computational and experimentally-informed approaches may shed light on the application of our method(s) and the patterns and processes underlying the contribution of MH to gene evolution.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary shortcuts via multi-nucleotide substitutions and their impact on natural selection analyses

Lucaci

Zehr

Pond

2022

Preprint

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Inference and interpretation of evolutionary processes - in particular of the types and targets of natural selection affecting coding sequences, are critically influenced by the assumptions built into statistical models for such analyses. If certain aspects of the substitution process (even when they are not of direct interest) are presumed absent or are modeled with too crude of a simplification, estimates of key model parameters can become biased - often systematically, and lead to poor statistical performance. Here, we performed a detailed characterization of how modeling instantaneous multi-nucleotide (or multi-hit, MH) substitutions impacts dN/dS based inference of episodic diversifying selection at the level of the entire alignment. The inclusion of MH reduces the rate (1.37-fold or 26.8%) at which positive selection is called based on the analysis of N = 9,861 empirical data-sets, while offering significantly better statistical fit to sequence data in 8.37% of cases. Through additional simulation studies, we show that this reduction is not simply due to loss of power because of additional model complexity. After a detailed examination of 21 benchmark alignments and a new high-resolution analysis showing which parts of the alignment provide support for positive selection, we reveal that MH substitutions occurring along shorter branches in the tree are largely responsible for discrepant results in selection detection. Our results add to the growing body of literature which examines decades-old modeling assumptions and finds them to be problematic for biological data analysis. Because multi-nucleotide substitutions have a significant impact on natural selection detection even at the level of an entire gene, we recommend that routine selection analysis of this type consider their inclusion. To facilitate this procedure, we developed a simple model testing selection detection framework able to screen an alignment for positive selection with two biologically important confounding processes: synonymous rate variation, and multi-nucleotide instantaneous substitutions.

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Alternative splicing in seasonal plasticity and the potential for adaptation to environmental change

Cited by 41 publications

References 93 publications

Elevated temperatures reduce population‐specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Elevated temperatures reduce population‐specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Elevated temperatures reduce population-specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Evolutionary shortcuts via multi-nucleotide substitutions and their impact on natural selection analyses

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