The Evolutionary Relationship between Alternative Splicing and Gene Duplication

Íñiguez, Luis P.; Hernández, Georgina

doi:10.3389/fgene.2017.00014

Cited by 55 publications

(55 citation statements)

References 54 publications

(55 reference statements)

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“…Interestingly, we observed that a paralog of U2AF2 on LG 33 was differentially expressed between ecotypes. This suggests that paralogs, which potentially originated through the whole-genome duplication in salmonids (Lien et al 2016), might be regulated through different molecular processes, thus increasing functional diversity while minimising constraints (Bush et al 2017;Iñiguez and Hernández 2017). A similar pattern was observed for MYH.…”

Section: Alternative Splicing and Gene Expression Have Contrasting Phmentioning

confidence: 81%

“…A similar pattern was observed for MYH. However, more analyses are needed to test this pattern (Iñiguez and Hernández 2017) and assess the role of the whole-genome duplication in salmonids on the regulatory divergence between recently diverged ecotypes. Without detailed molecular studies of translation, protein abundance and transcript decay for candidate genes, we cannot discern the exact molecular and phenotypic impact of splicing and expression events (Mallarino et al 2017).…”

Section: Alternative Splicing and Gene Expression Have Contrasting Phmentioning

confidence: 99%

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Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish

Jacobs

Elmer

2020

Preprint

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Understanding the contribution of different molecular processes to the evolution and development of divergent phenotypes is crucial for identifying the molecular routes of rapid adaptation. Here, we used RNA-seq data to compare patterns of alternative splicing and differential gene expression in a case of parallel adaptive evolution, the replicated postglacial divergence of the salmonid fish Arctic charr (Salvelinus alpinus) into benthic and pelagic ecotypes across multiple independent lakes.We found that genes that were differentially spliced and differentially expressed between the benthic and pelagic ecotypes were mostly independent (<6% overlap) and were involved in different processes. Differentially spliced genes were primarily enriched for muscle development and functioning, while differentially expressed genes were mostly involved in energy metabolism, immunity and growth. Together, these likely explain different axes of divergence between ecotypes in swimming performance and activity. Furthermore, we found that alternative splicing and gene expression are mostly controlled by independent cis-regulatory quantitative trait loci (<3.4% overlap). Cis-regulatory regions were associated with the parallel divergence in splicing (16.5% of intron clusters) and expression (6.7 -10.1% of differentially expressed genes), indicating shared regulatory variation across ecotype pairs. Contrary to theoretical expectation, we found that differentially spliced genes tended to be highly central in regulatory networks ('hub genes') andwere annotated to significantly more gene ontology terms compared to non-differentially spliced genes, consistent with a higher level of connectivity and pleiotropy.Together, our results suggest that the concerted regulation of alternative splicing and differential gene expression through different regulatory regions leads to the divergence of complementary phenotypes important for local adaptation. This study provides novel insights into the importance of contrasting but putatively complementary molecular processes for rapid and parallel adaptive evolution.Bush et al. 2017), or alter the regulation of transcript abundance through the formation of nonsense transcripts, which will be efficiently removed (Aznarez et al. 2018;Grantham and Brisson 2018). In eukaryotes, the majority of genes undergo splicing at some point during development (Grau-Bové et al. 2018). Splicing occurs through a dynamic ribonucleoprotein complex, the spliceosome (Lee and Rio 2015) and studies in model organisms showed that the expression and splicing of genes are mostly controlled by different genetic loci, indicating these processes can evolve independently (Li et al. 2016). Patterns of alternative splicing have been found to differ between closely-related species (Harr and Turner 2010;Singh et al. 2017) and the differential splicing of individual genes has in some cases been linked to the rapid evolution of ecologically-relevant phenotypic traits (Howes et al. 2017;Mallarino et al. 2017). In principle, alternative spli...

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Section: Alternative Splicing and Gene Expression Have Contrasting Phmentioning

confidence: 81%

Section: Alternative Splicing and Gene Expression Have Contrasting Phmentioning

confidence: 99%

Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish

Jacobs

Elmer

2020

Preprint

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“…Finally, DTU was compared between genes with a different number of paralogs to study the relationship between gene duplication and DTU. The relationship between gene duplication and AS has been studied extensively, but is not fully understood (Iniguez and Hernandez, ). Singleton genes in rice were found to produce less alternatively spliced isoforms than genes with paralogs (Lin et al ., ), but for human genes the reverse trend was observed (Roux and Robinson‐Rechavi, ).…”

Section: Resultsmentioning

confidence: 99%

“…Full enrichment results can be found in Table S3. studied extensively, but is not fully understood (Iniguez and Hernandez, 2017). Singleton genes in rice were found to produce less alternatively spliced isoforms than genes with paralogs (Lin et al, 2008), but for human genes the reverse trend was observed (Roux and Robinson-Rechavi, 2011).…”

Section: Cds Altering Dtu Occurs Disproportionately Across Genes Withmentioning

confidence: 99%

Genome‐wide characterization of differential transcript usage in Arabidopsis thaliana

et al. 2017

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Alternative splicing and the usage of alternate transcription start- or stop sites allows a single gene to produce multiple transcript isoforms. Most plant genes express certain isoforms at a significantly higher level than others, but under specific conditions this expression dominance can change, resulting in a different set of dominant isoforms. These events of differential transcript usage (DTU) have been observed for thousands of Arabidopsis thaliana, Zea mays and Vitis vinifera genes, and have been linked to development and stress response. However, neither the characteristics of these genes, nor the implications of DTU on their protein coding sequences or functions, are currently well understood. Here we present a dataset of isoform dominance and DTU for all genes in the AtRTD2 reference transcriptome based on a protocol that was benchmarked on simulated data and validated through comparison with a published reverse transciptase-polymerase chain reaction panel. We report DTU events for 8148 genes across 206 public RNA-Seq samples, and find that protein sequences are affected in 22% of the cases. The observed DTU events show high consistency across replicates, and reveal reproducible patterns in response to treatment and development. We also demonstrate that genes with different evolutionary ages, expression breadths and functions show large differences in the frequency at which they undergo DTU, and in the effect that these events have on their protein sequences. Finally, we showcase how the generated dataset can be used to explore DTU events for genes of interest or to find genes with specific DTU in samples of interest.

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“…Cells can generate multiple messenger RNAs (mRNAs) with different functions from a single genomic gene through alternative splicing [29], [30]. Types of alternative splicing include the use of alternative 5′ splice sites (alternative donor), alternative 3′ splice sites (alternative acceptor AA), exon skipping, intron retention and mutually exclusive exons (Figure 2) [31]. In addition, new discoveries have shed light into the mechanisms responsible for the production of circular RNAs (circRNAs), which imply alternative splicing [32]-[34].…”

Section: B-splicingmentioning

confidence: 99%

IDENTIFICATION OF RNA STRUCTURES MODULATING THE EXPRESSION OF THE mRNA BIOGENESIS FACTOR SUS1

AbuQattam¹

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The Evolutionary Relationship between Alternative Splicing and Gene Duplication

Cited by 55 publications

References 54 publications

Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish

Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish

Genome‐wide characterization of differential transcript usage in Arabidopsis thaliana

IDENTIFICATION OF RNA STRUCTURES MODULATING THE EXPRESSION OF THE mRNA BIOGENESIS FACTOR SUS1

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