Environmental Stresses Modulate Abundance and Timing of Alternatively Spliced Circadian Transcripts in Arabidopsis

Abstract

Environmental stresses profoundly altered accumulation of nonsense mRNAs including intron retaining (IR) transcripts in Arabidopsis. Temporal patterns of stress-induced IR mRNAs were dissected using both oscillating and non-oscillating transcripts. Broad range thermal cycles triggered a sharp increase in the long intron retaining CCA1 isoforms and altered their phasing to different times of day. Both abiotic and biotic stresses such as drought or P. syringae infection induced similar increase. Thermal stress induced a time delay in accumulation of CCA1 I4Rb transcripts whereas functional mRNA showed steady oscillations. Our data favor a hypothesis that stress-induced instabilities of the central oscillator can be in part compensated through fluctuations in abundance and out of phase oscillations of CCA1 IR transcripts. Altogether, our results support a concept that mRNA abundance can be modulated through altering ratios between functional and nonsense/IR transcripts. SR45 protein specifically bound to the retained CCA1 intron in vitro, suggesting that this splicing factor could be involved in regulation of intron retention. Transcriptomes of NMD-impaired and heat-stressed plants shared a set of retained introns associated with stress- and defense-inducible transcripts. Constitutive activation of certain stress response networks in an NMD mutant could be linked to disequilibrium between functional and nonsense mRNAs.

High temperature attenuates the gravitropism of inflorescence stems by inducing SHOOT GRAVITROPISM 5 alternative splicing in Arabidopsis

“…Alternative splicing via the retention of intron is involved in the diverse aspects of plant responses to environmental stress (Seo et al ., , , ; Chang et al ., ; Kwon et al ., ; Filichkin et al ., ). A question was whether the effects of high temperatures on SGR5 alternative splicing are specific or simply reflect heat stress‐induced disruption of the splicing machinery.…”

3′-Phosphoadenosine 5′-Phosphate Accumulation Delays the Circadian System

“…The importance of posttranscriptional regulation of circadian gene expression is increasingly being recognized, particularly in response to environmental changes (Garbarino-Pico and Green, 2007;Kojima et al, 2011;Sanchez et al, 2011b). Misregulation of RNA processing frequently leads to an altered circadian FRP (Jones et al, 2012;Wang et al, 2012;MacGregor et al, 2013;Perez-Santángelo et al, 2014) and alternate splicing contributes to modifications to the circadian system in response to temperature and drought (James et al, 2012;Filichkin et al, 2015). Similarly, circadian regulation of exosome activity has previously been implicated in the circadian system of the bread mold Neurospora crassa (Guo et al, 2009;Zhang et al, 2015).…”

Transcriptional networks — crops, clocks, and abiotic stress

“…Although GCNs provide valuable insight into pathway regulation, they cannot differentiate between transcriptional co-regulation and post-transcriptional modification of steady state levels which has been shown to be especially relevant for circadian clock-mediated stress response [72,73]. The most attractive applicability of GCNs is their utility for building predictive models that integrate protein-protein interactions, TF-cis-element interactions, microRNA-mRNA interactions, alternative splicing dynamics and other '-omic' datasets for inferring causality.…”