SKIP regulates environmental fitness and floral transition by forming two distinct complexes in Arabidopsis

Abstract

Summary Ski‐interacting protein (SKIP) is a bifunctional regulator of gene expression that works as a splicing factor as part of the spliceosome and as a transcriptional activator by interacting with EARLY FLOWERING 7 (ELF7). MOS4‐Associated Complex 3A (MAC3A) and MAC3B interact physically and genetically with SKIP, mediate the alternative splicing of c. 50% of the expressed genes in the Arabidopsis genome, and are required for the splicing of a similar set of genes to that of SKIP. SKIP interacts physically and genetically with splicing factors and Polymerase‐Associated Factor 1 complex (Paf1c) components. However, these splicing factors do not interact either physically or genetically with Paf1c components. The SKIP‐spliceosome complex mediates circadian clock function and abiotic stress responses by controlling the alternative splicing of pre‐mRNAs encoded by clock‐ and stress tolerance‐related genes. The SKIP‐Paf1c complex regulates the floral transition by activating FLOWERING LOCUS C (FLC) transcription. Our data reveal that SKIP regulates floral transition and environmental fitness via its incorporation into two distinct complexes that regulate gene expression transcriptionally and post‐transcriptionally, respectively. It will be interesting to discover in future studies whether SKIP is required for integration of environmental fitness and growth by control of the incorporation of SKIP into spliceosome or Paf1c in plants.

To Splice or to Transcribe: SKIP-Mediated Environmental Fitness and Development in Plants

“…Therefore, SKIP mediates the circadian clock by regulating the alternative splicing of clock genes. These findings demonstrate that post-transcriptional regulation plays vital roles in controlling the circadian clock (Sanchez et al, 2010; Jones et al, 2012; Wang et al, 2012; Li et al, 2019).…”

“…Thus, SKIP is not required for the accurate splicing of FLC or COOLAIR pre-mRNA. Instead, FLC transcription (i.e., the level of unspliced FLC mRNA) is significantly repressed in skip-1 ; this is reflected in the obvious repression of mature FLC transcripts and the early flowering phenotype observed in skip-1 under different photoperiod and temperature conditions (Cao et al, 2015; Li et al, 2016; Li et al, 2019). Thus, SKIP activates FLC expression at the transcriptional level in a photoperiod- and temperature-independent manner, and it represses flowering time by promoting FLC transcription.…”

“…SKIP also regulates plant response to abiotic stress (Hou et al, 2009; Zhang Y, et al, 2013; Feng et al, 2015; Li et al, 2016; Li et al, 2019). Mutations in SKIP have been shown to cause hypersensitivity to salt or osmotic stress in Arabidopsis .…”

“…Transcripts of several salt tolerance-related genes, including NA + /H + EXCHANGER 1 ( NHX1 ), CALCINEURIN B-LIKE PROTEIN 1 ( CBL1 ), DELTA1-PYRROLINE-5-CARBOXYLATE SYNTHASE 1 ( P5CS1 ), RARE-COLD-INDUCIBLE 2A ( RCI2A ), and PROTEIN S-ACYL TRANSFERASE 10 ( PAT10 ), are aberrantly spliced in skip-1 under salt stress conditions, decreasing the abundance of fully spliced mRNAs. Premature termination during the translation of these aberrantly spliced variants in skip-1 reduces the level of functional proteins, resulting in salt hypersensitivity (Feng et al, 2015; Li et al, 2016; Li et al, 2019). Therefore, SKIP is necessary for plants to respond to salt or drought stress, and alternative gene splicing is crucial for plants to respond to environmental cues (Hou et al, 2009; Zhang Y, et al, 2013; Feng et al, 2015; Li et al, 2016; Li et al, 2019; reviewed in Filichkin et al, 2015; Laloum et al, 2018).…”

“…SKIP has a dual function in plants: it acts as a splicing factor to control efficient and precise pre-mRNA splicing on a genome-wide scale by interacting with other spliceosome components (e.g., SR45) and integrating into the spliceosome, and it is required for 5′ and 3′ splice site recognition or cleavage (Wang et al, 2012; Feng et al, 2015). SKIP affects the circadian clock and plant responses to salt stress by regulating the accurate splicing of certain clock- and salt tolerance-related genes (Wang et al, 2012; Feng et al, 2015; Li et al, 2016; Li et al, 2019). SKIP also functions as a transcriptional co-regulator by interacting with other transcriptional regulators (e.g., Paf1c), and it mediates the floral transition (Cao et al, 2015; Li et al, 2016; Li et al, 2019).…”