SKIP Confers Osmotic Tolerance during Salt Stress by Controlling Alternative Gene Splicing in Arabidopsis

Feng, Jinlin; Li, Jingjing; Gao, Zhaoxu; Lu, Yaru; Yu, Junya; Zheng, Qian; Yan, Shuning; Zhang, Wenjiao; He, Hang; Ma, Ligeng; Zhang, Zhu

doi:10.1016/j.molp.2015.01.011

Cited by 137 publications

(165 citation statements)

References 62 publications

(111 reference statements)

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“…In plants, we previously reported that SKIP interacts with ELF7, a core component of the Paf1 complex (Paf1c) (He et al ., ), to form the SKIP‐ELF7, which activates the transcription of FLC and MAF1‐5 and represses the floral transition in Arabidopsis (Cao et al ., ; Y. Li et al ., ). We also confirmed that SKIP is a component of the spliceosome, and that it is required for the genome‐wide splicing of pre‐mRNAs and proper functioning of the circadian clock and abiotic stress response in Arabidopsis via the regulated splicing of clock‐ and stress tolerance‐related genes (Wang et al ., ; Feng et al ., ; Y. Li et al ., ).…”

Section: Introductionmentioning

confidence: 99%

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

Yang

Shang

et al. 2019

New Phytologist

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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.

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Section: Introductionmentioning

confidence: 99%

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

Yang

Shang

et al. 2019

New Phytologist

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“…Moreover, SR45 has been found to interact with three U5 small nuclear ribonucleoprotein proteins (Zhang et al, 2014) as well as with several other Arabidopsis SR proteins, namely, SCL33, RSZ21, SR30, SR34, and SR34a (Golovkin and Reddy, 1999;Zhang et al, 2014;Stankovic et al, 2016). Two other reported SR45-interacting proteins in Arabidopsis are the spliceosomal component SKIP (Wang et al, 2012), which confers salt stress tolerance (Feng et al, 2015), and CACTIN, an essential nuclear factor required for embryogenesis (Baldwin et al, 2013). Early studies had shown that AFC2, a LAMMER-type protein kinase, is able to interact with and phosphorylate SR45 in vitro (Golovkin and Reddy, 1999) and found SR45 to be confined to the nucleus, either diffusely distributed in the nucleoplasm or concentrated in speckles, with its subnuclear dynamics being regulated by phosphorylation, ATP, and transcription (Ali et al, 2003;Ali and Reddy, 2006).…”

Section: Introductionmentioning

confidence: 99%

The Arabidopsis SR45 Splicing Factor, a Negative Regulator of Sugar Signaling, Modulates SNF1-Related Protein Kinase 1 Stability

et al. 2016

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The ability to sense and respond to sugar signals allows plants to cope with environmental and metabolic changes by adjusting growth and development accordingly. We previously reported that the SR45 splicing factor negatively regulates glucose signaling during early seedling development in Arabidopsis thaliana. Here, we show that under glucose-fed conditions, the Arabidopsis sr45-1 loss-of-function mutant contains higher amounts of the energy-sensing SNF1-Related Protein Kinase 1 (SnRK1) despite unaffected SnRK1 transcript levels. In agreement, marker genes for SnRK1 activity are upregulated in sr45-1 plants, and the glucose hypersensitivity of sr45-1 is attenuated by disruption of the SnRK1 gene. Using a high-resolution RT-PCR panel, we found that the sr45-1 mutation broadly targets alternative splicing in vivo, including that of the SR45 pre-mRNA itself. Importantly, the enhanced SnRK1 levels in sr45-1 are suppressed by a proteasome inhibitor, indicating that SR45 promotes targeting of the SnRK1 protein for proteasomal destruction. Finally, we demonstrate that SR45 regulates alternative splicing of the Arabidopsis 5PTase13 gene, which encodes an inositol polyphosphate 5-phosphatase previously shown to interact with and regulate the stability of SnRK1 in vitro, thus providing a mechanistic link between SR45 function and the modulation of degradation of the SnRK1 energy sensor in response to sugars.

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“…Here, the results showed that although expression of VvPMA1 α was higher than VvPMA1 β expression in root, regardless of treatment (Figures 7A,B), the expression level of VvPMA1 β still greatly increased under salt stress, suggesting that alternative splicing of VvPMA1 was markedly induced under salt conditions. Previous results showed that splicing factors, such as serine/arginine-rich (SR), Ski-interacting protein (SKIP) etc., can control the AS of pre-mRNAs encoded by salt tolerance genes under salt stress in plants (Syed et al, 2012; Feng et al, 2015) and different growth conditions can modulate gene expression or protein modification of splicing factors causing dynamic changes in the splicing factor profile, further impacting expression of target genes. So we supposed that the expression of spliced variant VvPMA1 β must be controlled by one or some specific splicing factors in grape root under salt conditions, moreover, VvPMA1 β expression maintained low level in root under salt stress probably because the specific splicing factor has weak activity.…”

Section: Discussionmentioning

confidence: 99%

Identification of a Novel Alternative Splicing Variant of VvPMA1 in Grape Root under Salinity

Han

et al. 2017

Front. Plant Sci.

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It has been well-demonstrated that the control of plasma membrane H+-ATPase (PM H+-ATPase) activity is important to plant salt tolerance. This study found a significant increase in PM H+-ATPase (PMA) activity in grape root exposed to NaCl. Furthermore, 7 Vitis vinifera PM H+-ATPase genes (VvPMAs) were identified within the grape genome and the expression response of these VvPMAs in grape root under salinity was analyzed. Two VvPMAs (VvPMA1 and VvPMA3) were expressed more strongly in roots than the other five VvPMAs. Moreover, roots exhibited diverse patterns of gene expression of VvPMA1 and VvPMA3 responses to salt stress. Interestingly, two transcripts of VvPMA1, which were created through alternative splicing (AS), were discovered and isolated from salt stressed root. Comparing the two VvPMA1 cDNA sequences (designated VvPMA1α and VvPMA1β) with the genomic sequence revealed that the second intron was retained in the VvPMA1β cDNA. This intron retention was predicted to generate a novel VvPMA1 through N-terminal truncation because of a 5′- terminal frame shift. Yeast complementation assays of the two splice variants showed that VvPMA1β could enhance the ability to complement Saccharomyces cerevisiae deficient in PM H+-ATPase activity. In addition, the expression profiles of VvPMA1α and VvPMA1β differed under salinity. Our data suggests that through AS, the N-terminal length of VvPMA1 may be regulated to accurately modulate PM H+-ATPase activity of grape root in salt stress.

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SKIP Confers Osmotic Tolerance during Salt Stress by Controlling Alternative Gene Splicing in Arabidopsis

Cited by 137 publications

References 62 publications

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

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

The Arabidopsis SR45 Splicing Factor, a Negative Regulator of Sugar Signaling, Modulates SNF1-Related Protein Kinase 1 Stability

Identification of a Novel Alternative Splicing Variant of VvPMA1 in Grape Root under Salinity

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