Alternative splicing (AS) increases gene expression complexity by producing diverse protein coding transcripts from a single precursor-messenger RNA (pre-mRNA). Studies exploring transcript diversity in Arabidopsis thaliana (Arabidopsis) estimate approximately 60% of protein-coding genes to be alternatively spliced [[1], [2], [3], [4]]. Pre-mRNA splicing is catalyzed by dynamic macromolecular ribonucleoprotein (RNP) complexes, together constituting the spliceosome [5,6]. The major spliceosome consists of five RNA-protein complexes, designated the U1, U2, U4, U5, and U6 small nuclear ribonucleoproteins (snRNPs) that bind uridine-rich small nuclear RNA (snRNA) and include Smith antigen (Sm) proteins and other associated proteins [7]. The seven evolutionary conserved Sm proteins (B, D1, D2, D3, E, F, and G) are surrounding the snRNA in a heptameric ring-shaped complex via a bipartite Sm sequence motif [5,8,9]. The Sm ring and snRNPs are assembled in a multi-step pathway mediated by the survival motor neuron (SMN) complex [10]. Next to Sm proteins, eight ‘Like-Sm’ (LSm) proteins form two different heptameric complexes: the LSm2-8 complex, a component of the U6 snRNP performing pre-mRNA splicing [11,12], and the LSm1-7 complex involved in mRNA decapping [13].

In plants, AS is an important posttranscriptional regulation mechanism in response to environmental perturbations [4]. Accordingly, thousands of pre-mRNAs of genes are alternatively spliced during cold acclimation [14], salt stress [15], drought and heat stresses [16]. Concomitantly, Arabidopsis splicing-related proteins themselves regulate pre-mRNA splicing activity in a stress dependent manner [4,15,17,18]. For instance, LSm8 mutation caused differential splicing under stress, correlating with improved cold and hypersensitivity to salt stress, thereby indicating an environment dependent regulation by the LSm2-8 complex [18]. Besides the LSm2-8 complex, also Sm proteins and proteins facilitating snRNP assembly have been associated with stress responses. A mutation of SmD3-b and the snRNP assembly proteins PRMT5 and ICLN results in increased resistance to a virulent oomycete in Arabidopsis [19]. And, more recently, the Sm protein SME1 was associated with low temperature acclimation, with loss-of-function mutants displaying developmental defects at lower temperatures [20,21].

So far, our lab identified in a second-site suppressor screen mutations of the metabolic enzyme GLYCOLATE OXIDASE2 and the transcription factor SHORT-ROOT to alleviate photorespiratory cell death in catalase (cat2-2) deficient plants [22,23]. Under photorespiration-promoting growth conditions, Arabidopsis mutants deficient in the hydrogen peroxide (H2O2)-scavenging CATALASE2 (cat2-2) display a loss of PSII maximum efficiency (Fv'/Fm’) and develop cell death lesions [24,25]. Here, we describe a nonsense mutation in SME1 that suppresses cat2-2 dependent cell death and exhibits a constitutively activated stress response associated with an enhanced tolerance to the ROS stimulating herbicide methyl viologen. mRNA-seq analysis of sme1-2 mutants revealed pre-mRNA splicing alterations, of which intron retention was the predominant AS event. In a tandem affinity purification (TAP) experiment using SME1 as a bait, almost 50 characterized or hypothesized components of the plant spliceosome were detected. Similarly to SME1 mutation, mutation of one of its interactors ICLN, involved in snRNP assembly, resulted in stunted growth under low temperatures and enhanced tolerance to methyl viologen. Taken together, our results suggest that perturbation of the Sm protein SME1 or snRNP assembly triggers a constitutive stress response enabling resilience to oxidative stress.