Regulation of alternative splicing in response to temperature variation in plants

Abstract

Plants have evolved numerous molecular strategies to cope with perturbations in environmental temperature, and to adjust growth and physiology to limit the negative effects of extreme temperature. One of the strategies involves alternative splicing of primary transcripts to encode alternative protein products or transcript variants destined for degradation by nonsense-mediated decay. Here, we review how changes in environmental temperature-cold, heat, and moderate alterations in temperature-affect alternative splicing in plants, including crops. We present examples of the mode of action of various temperature-induced splice variants and discuss how these alternative splicing events enable favourable plant responses to altered temperatures. Finally, we point out unanswered questions that should be addressed to fully utilize the endogenous mechanisms in plants to adjust their growth to environmental temperature. We also indicate how this knowledge might be used to enhance crop productivity in the future.

Keywords: Alternative splicing; ambient temperature; cold; heat; plants; stress adaptation.

Fig. 1.

Alternative splicing (AS) events in plants. (A) Types of splicing events (see also Verhage et al., (2017)). (B) Percentage of different AS events reported to date in response to cold, changes in ambient temperature, and heat in plants. Data were extracted from PubMed Central, December 2020 (https://pubmed.ncbi.nlm.nih.gov/). A3SS, alternative 3′ splice site selection; A5SS, alternative 5′ splice site selection; ES, exon skipping; IR, intron retention; MXE, mutual exclusion of exons.

Fig. 2.

Role of temperature-induced alternative splicing (AS) and mode of action of different splice variants. (A) Regulation of down-stream target genes when the transcription factor (TF) transcript undergoes constitutive splicing to form a functional protein. A functional homodimer of the TF is formed that binds to the promoters of target genes to activate or repress their expression. (B) Temperature-induced AS can lead to three types of TF regulation. (i) Peptide interference by the formation of small interfering peptides (siPEPs). The alternatively spliced mRNA leads to a truncated protein that functions as an siPEP by forming a non-functional heterodimer with the functional protein; this inhibits the TF from binding to the promoters of target genes to affect their expression. (ii) Nonsense-mediated decay (NMD) of alternatively spliced transcripts. Many splice variants that contain premature termination codons (PTCs) are targeted for degradation by NMD, thereby altering the transcript levels available for translation to form the functional TF protein. (iii) Activation of the TF. AS leads to the formation of a truncated protein that has the ability to bind to the promoter of its own gene and modify its expression. Red lines represent constitutive splicing and orange lines represent temperature-induced AS.

Fig. 3.

Temperature-induced alternative splicing (AS) under different temperature conditions resulting in the plant’s adaptation. Overview of the genes undergoing AS under diverse temperature regimes like cold (around 4–15 °C), changes in ambient temperature (16–27 °C), and heat stress (28–45 °C), and the resulting physiological responses. AS in response to changes in temperature (including extreme temperatures) has been shown to play an important role in improving plant performance and stress tolerance. As an example, AS of the flowering time genes FLM and MAF2 in response to a change in ambient temperature regulates the transition to flowering and reproductive growth in plants. A higher ambient temperature (27 °C) induces flowering while a lower temperature (16 °C) represses flowering. Dashed lines indicate indirect responses. The red arrows indicate up-regulation (upward arrow) or down-regulation (downward arrow). IR, intron retention; MXI, mutually exclusive incorporation; NMD, non-sense mediated decay; siPEPs, small interfering peptides.