Does co-transcriptional regulation of alternative splicing mediate plant stress responses?

Abstract

Plants display exquisite control over gene expression to elicit appropriate responses under normal and stress conditions. Alternative splicing (AS) of pre-mRNAs, a process that generates two or more transcripts from multi-exon genes, adds another layer of regulation to fine-tune condition-specific gene expression in animals and plants. However, exactly how plants control splice isoform ratios and the timing of this regulation in response to environmental signals remains elusive. In mammals, recent evidence indicate that epigenetic and epitranscriptome changes, such as DNA methylation, chromatin modifications and RNA methylation, regulate RNA polymerase II processivity, co-transcriptional splicing, and stability and translation efficiency of splice isoforms. In plants, the role of epigenetic modifications in regulating transcription rate and mRNA abundance under stress is beginning to emerge. However, the mechanisms by which epigenetic and epitranscriptomic modifications regulate AS and translation efficiency require further research. Dynamic changes in the chromatin landscape in response to stress may provide a scaffold around which gene expression, AS and translation are orchestrated. Finally, we discuss CRISPR/Cas-based strategies for engineering chromatin architecture to manipulate AS patterns (or splice isoforms levels) to obtain insight into the epigenetic regulation of AS.

Alternative Splicing and DNA Damage Response in Plants

“…The secondary structure of the pre-mRNA can alter access to splicing signals and binding sites for splicing factors (SFs) or change the distance between these elements (Shepard and Hertel, 2008). Differential DNA methylation, histone modifications, and nucleosome positioning modulate RNA polymerase II elongation speed and recruitment of SFs, thus also resulting in alternative splice site selection [for a recent review see (Jabre et al, 2019)].…”

AnArabidopsislong noncoding RNA modulates the transcriptome through interactions with a network of splicing factors

“…In humans, numerous studies suggest that the misregulation of RNA splicing is associated to several diseases (Boon et al, 2007;Tanackovic et al, 2011;Yoshida et al, 2011;Faial, 2015). In plants, AS plays an important role in the control of gene expression for an adequate response of plants to stress conditions (Palusa et al, 2007;Tanabe et al, 2007;Filichkin et al, 2010;Yan et al, 2012;Reddy et al, 2013;Ding et al, 2014;Zhan et al, 2015;Laloum et al, 2018;Jabre et al, 2019;Rigo et al, 2019). Alternative splicing modulates gene expression mainly by (i) increasing gene-coding capacity, thus proteome complexity, through the generation of a subset of mRNA isoforms derived from a single locus, and/or (ii) triggering mRNA degradation through the introduction of a premature termination codon in specific isoforms that would lead to nonsense mediated decay (NMD).…”

Mimulus sRNAs Are Wound Responsive and Associated with Transgenerationally Plastic Genes but Rarely Both

“…These programs can leave a lasting epigenetic mark on the genome in cells that have received developmental or environmental signals. These lasting epigenetic modifications include DNA methylation, histone methylation and histone acetylation and can alter the RNA expression, chromatin accessibility and splicing that occurs proximal to these markings [ 1 , 2 , 3 ]. Additionally, these markings can be transmitted between mitotic and sometimes meiotic cell divisions [ 4 , 5 ] allowing developmental and environmental cues to leave a lasting impact on a cell lineage, altering the development of cells in later life history stages or even in the next generation.…”