Arabidopsis RNA processing factor SERRATE regulates the transcription of intronless genes
- University of Tübingen, Germany
- Umeå University, Sweden
Abstract
Intron splicing increases proteome complexity, promotes RNA stability, and enhances transcription. However, introns and the concomitant need for splicing extend the time required for gene expression and can cause an undesirable delay in the activation of genes. Here, we show that the plant microRNA processing factor SERRATE (SE) plays an unexpected and pivotal role in the regulation of intronless genes. Arabidopsis SE associated with more than 1000, mainly intronless, genes in a transcription-dependent manner. Chromatin-bound SE liaised with paused and elongating polymerase II complexes and promoted their association with intronless target genes. Our results indicate that stress-responsive genes contain no or few introns, which negatively affects their expression strength, but that some genes circumvent this limitation via a novel SE-dependent transcriptional activation mechanism. Transcriptome analysis of a Drosophila mutant defective in ARS2, the metazoan homologue of SE, suggests that SE/ARS2 function in regulating intronless genes might be conserved across kingdoms.
Data availability
Raw data have been deposited under accession codes accession number ERP016859 (ENA), PXD006004 (Pride) and GSE99367 (Geo Omnibus).
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RNA-seq of se mutantsPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE99367).
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Transcriptomic comparison of Drosophila snRNP biogenesis mutants reveals mutant-specific changes in pre-mRNA processing: implications for Spinal Muscular AtrophyPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE81121).
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RNA-Seq analysis, transcriptome assembly and gene expression profile analysis for Zea may ssp. mexicana L. under cold and drought stressPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE76939).
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Comprehensive characterization and RNA-Seq profiling of the HD-Zip transcription factor family in soybean (Glycine max) during dehydration and salt stressPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE57252).
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft
- Sascha Laubinger
Max-Planck-Gesellschaft (Open-access funding)
- Sven zur Oven-Krockhaus
- York-Dieter Stierhof
- Sascha Laubinger
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2018, Speth et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Arabidopsis RNA processing factor SERRATE regulates the transcription of intronless genes
eLife 7:e37078.
https://doi.org/10.7554/eLife.37078
Further reading
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Meiotic crossover recombination is essential for both accurate chromosome segregation and the generation of new haplotypes for natural selection to act upon. This requirement is known as crossover assurance and is one example of crossover control. While the conserved role of the ATPase, PCH-2, during meiotic prophase has been enigmatic, a universal phenotype when pch-2 or its orthologs are mutated is a change in the number and distribution of meiotic crossovers. Here, we show that PCH-2 controls the number and distribution of crossovers by antagonizing their formation. This antagonism produces different effects at different stages of meiotic prophase: early in meiotic prophase, PCH-2 prevents double-strand breaks from becoming crossover-eligible intermediates, limiting crossover formation at sites of initial double-strand break formation and homolog interactions. Later in meiotic prophase, PCH-2 winnows the number of crossover-eligible intermediates, contributing to the designation of crossovers and ultimately, crossover assurance. We also demonstrate that PCH-2 accomplishes this regulation through the meiotic HORMAD, HIM-3. Our data strongly support a model in which PCH-2’s conserved role is to remodel meiotic HORMADs throughout meiotic prophase to destabilize crossover-eligible precursors and coordinate meiotic recombination with synapsis, ensuring the progressive implementation of meiotic recombination and explaining its function in the pachytene checkpoint and crossover control.
