Arabidopsis SME1 Regulates Plant Development and Response to Abiotic Stress by Determining Spliceosome Activity Specificity

Abstract

J.A.J.); 0000-0003-2020-0950 (J.S.)The control of precursor-messenger RNA (pre-mRNA) splicing is emerging as an important layer of regulation in plant responses to endogenous and external cues. In eukaryotes, pre-mRNA splicing is governed by the activity of a large ribonucleoprotein machinery, the spliceosome, whose protein core is composed of the Sm ring and the related Sm-like 2-8 complex. Recently, the Arabidopsis (Arabidopsis thaliana) Sm-like 2-8 complex has been characterized. However, the role of plant Sm proteins in pre-mRNA splicing remains largely unknown. Here, we present the functional characterization of Sm protein E1 (SME1), an Arabidopsis homolog of the SME subunit of the eukaryotic Sm ring. Our results demonstrate that SME1 regulates the spliceosome activity and that this regulation is controlled by the environmental conditions. Indeed, depending on the conditions, SME1 ensures the efficiency of constitutive and alternative splicing of selected pre-mRNAs. Moreover, missplicing of most targeted pre-mRNAs leads to the generation of nonsense-mediated decay signatures, indicating that SME1 also guarantees adequate levels of the corresponding functional transcripts. In addition, we show that the selective function of SME1 in ensuring appropriate gene expression patterns through the regulation of specific pre-mRNA splicing is essential for adequate plant development and adaptation to freezing temperatures. These findings reveal that SME1 plays a critical role in plant development and interaction with the environment by providing spliceosome activity specificity.

Characterization of novel regulators for heat stress tolerance in tomato from Indian sub‐continent

“…KEGG pathways like protein processing in ER, spliceosome and ubiquitin-mediated proteolysis were enriched in conserved upregulated genes (Table S3). Many recent reports on stressresponsive regulation of spliceosome per se, as well as, crucial role of alternatively spliced transcripts in response to abiotic stresses including HS have been reported in plants (Deng et al, 2011;Seo et al, 2012Seo et al, , 2013Carrasco-L opez et al, 2017;Calixto et al, 2018;Filichkin et al, 2018;Laloum et al, 2018;Huertas et al, 2019). The unfolded protein response (UPR) is a conserved response that is elicited by ER stress and is known to protect plants from adverse environmental stresses (Park and Park, 2019;Wan and Jiang, 2016).…”

First Come, First Served: Sui Generis Features of the First Intron

“…Sessile plants have adopted sophisticated mechanisms to adjust to the varying environment, and the regulation of AS appears to play a more pivotal role than previously assumed. Splicing efficiency is regulated by stresses such as abiotic stress [ 116 ], drought [ 117 ], salt [ 118 ], cold [ 119 , 120 ], high temperature [ 34 , 121 ] phytochrome B signaling [ 122 , 123 ] thermo-priming [ 124 ], temperature-dependent regulation of circadian clock genes [ 125 ], and phosphate starvation [ 126 ]. Vernalization is, in part, regulated by AS of FLC , a central repressor in the flowering transition [ 37 ].…”

Arabidopsis exoribonuclease USB1 interacts with the PPR-domain protein SOAR1 to negatively regulate abscisic acid signaling

“…In humans, processing of U6 by USB1 creates a terminal 2', 3'-cyclic phosphate which stimulates binding of U6 to a subunit of the spliceosome, the Sm-like (LSm) proteins 2–8, to form the U4/U6 snRNPs ( Licht et al , 2008 ; Hilcenko et al , 2013 ; Didychuk et al , 2016 ). The Arabidopsis homologues of human LSm, namely LSM2–LSM8, form a complex where LSM8 is a component of the U6 snRNP and were shown to be required for precursor mRNA splicing through U6 snRNA stabilization, which plays an important role in the environment-dependent regulation of spliceosome activity ( Perea-Resa et al , 2012 ; Carrasco-Lopez et al ., 2017 ; Huertas et al , 2019 ). The LSM1–LSM7 complex was reported to differentially regulate Arabidopsis tolerance to abiotic stress conditions by promoting selective mRNA decapping and especially by targeting to NCED3 and NCED5, two key enzymes in ABA biosynthesis ( Perea-Resa et al , 2016 ).…”