Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals
Abstract Background Alternative splicing (AS) is a widespread regulatory mechanism in multicellular organisms. Numerous transcriptomic and single-gene studies in plants have investigated AS in response to specific conditions, especially environmental stress, unveiling substantial amounts of intron r...
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doaj-6230ac0713e740fd8a4e672599787ea92021-01-17T12:56:31ZengBMCGenome Biology1474-760X2021-01-0122112610.1186/s13059-020-02258-yAlternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animalsGuiomar Martín0Yamile Márquez1Federica Mantica2Paula Duque3Manuel Irimia4Instituto Gulbenkian de CiênciaCentre for Genomic Regulation, Barcelona Institute of Science and TechnologyCentre for Genomic Regulation, Barcelona Institute of Science and TechnologyInstituto Gulbenkian de CiênciaCentre for Genomic Regulation, Barcelona Institute of Science and TechnologyAbstract Background Alternative splicing (AS) is a widespread regulatory mechanism in multicellular organisms. Numerous transcriptomic and single-gene studies in plants have investigated AS in response to specific conditions, especially environmental stress, unveiling substantial amounts of intron retention that modulate gene expression. However, a comprehensive study contrasting stress-response and tissue-specific AS patterns and directly comparing them with those of animal models is still missing. Results We generate a massive resource for Arabidopsis thaliana, PastDB, comprising AS and gene expression quantifications across tissues, development and environmental conditions, including abiotic and biotic stresses. Harmonized analysis of these datasets reveals that A. thaliana shows high levels of AS, similar to fruitflies, and that, compared to animals, disproportionately uses AS for stress responses. We identify core sets of genes regulated specifically by either AS or transcription upon stresses or among tissues, a regulatory specialization that is tightly mirrored by the genomic features of these genes. Unexpectedly, non-intron retention events, including exon skipping, are overrepresented across regulated AS sets in A. thaliana, being also largely involved in modulating gene expression through NMD and uORF inclusion. Conclusions Non-intron retention events have likely been functionally underrated in plants. AS constitutes a distinct regulatory layer controlling gene expression upon internal and external stimuli whose target genes and master regulators are hardwired at the genomic level to specifically undergo post-transcriptional regulation. Given the higher relevance of AS in the response to different stresses when compared to animals, this molecular hardwiring is likely required for a proper environmental response in A. thaliana.https://doi.org/10.1186/s13059-020-02258-yStress responsesTissue-specific transcriptomesGene regulationAlternative splicingAbiotic stressBiotic stress |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Guiomar Martín Yamile Márquez Federica Mantica Paula Duque Manuel Irimia |
spellingShingle |
Guiomar Martín Yamile Márquez Federica Mantica Paula Duque Manuel Irimia Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals Genome Biology Stress responses Tissue-specific transcriptomes Gene regulation Alternative splicing Abiotic stress Biotic stress |
author_facet |
Guiomar Martín Yamile Márquez Federica Mantica Paula Duque Manuel Irimia |
author_sort |
Guiomar Martín |
title |
Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals |
title_short |
Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals |
title_full |
Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals |
title_fullStr |
Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals |
title_full_unstemmed |
Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals |
title_sort |
alternative splicing landscapes in arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals |
publisher |
BMC |
series |
Genome Biology |
issn |
1474-760X |
publishDate |
2021-01-01 |
description |
Abstract Background Alternative splicing (AS) is a widespread regulatory mechanism in multicellular organisms. Numerous transcriptomic and single-gene studies in plants have investigated AS in response to specific conditions, especially environmental stress, unveiling substantial amounts of intron retention that modulate gene expression. However, a comprehensive study contrasting stress-response and tissue-specific AS patterns and directly comparing them with those of animal models is still missing. Results We generate a massive resource for Arabidopsis thaliana, PastDB, comprising AS and gene expression quantifications across tissues, development and environmental conditions, including abiotic and biotic stresses. Harmonized analysis of these datasets reveals that A. thaliana shows high levels of AS, similar to fruitflies, and that, compared to animals, disproportionately uses AS for stress responses. We identify core sets of genes regulated specifically by either AS or transcription upon stresses or among tissues, a regulatory specialization that is tightly mirrored by the genomic features of these genes. Unexpectedly, non-intron retention events, including exon skipping, are overrepresented across regulated AS sets in A. thaliana, being also largely involved in modulating gene expression through NMD and uORF inclusion. Conclusions Non-intron retention events have likely been functionally underrated in plants. AS constitutes a distinct regulatory layer controlling gene expression upon internal and external stimuli whose target genes and master regulators are hardwired at the genomic level to specifically undergo post-transcriptional regulation. Given the higher relevance of AS in the response to different stresses when compared to animals, this molecular hardwiring is likely required for a proper environmental response in A. thaliana. |
topic |
Stress responses Tissue-specific transcriptomes Gene regulation Alternative splicing Abiotic stress Biotic stress |
url |
https://doi.org/10.1186/s13059-020-02258-y |
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