Chemically-induced cellular stress signals are transmitted to alternative splicing via UsnRNA levels to alter gene expression in Arabidopsis thaliana

Alternative pre-mRNA splicing (AS) is a crucial regulatory layer of gene expression in eukaryotes. AS patterns can change in response to abiotic and biotic stress, allowing cellular functions to adapt to environmental conditions. Here, we examined the effects of cellular stress-inducing chemicals on AS-mediated gene regulation in Arabidopsis thaliana by investigating the alternatively spliced forms of SERINE-ARGININE PROTEIN30 (SRp30) and U1-70 K, encoding splicing factors, as well as ASCORBATE PEROXIDASE3 (APX3) and FOLYLPOLYGLUTAMATE SYNTHASE3 (FPGS3), encoding enzymes important for stress responses. Disrupting key cellular activities, including nitric oxide metabolism, ATPase activity, plastid function, and genome stability, affected AS patterns in Arabidopsis. Stress treatment altered the abundance of uridine-rich small nuclear RNAs (UsnRNAs), especially U1 snRNAs, which are essential non-coding RNA components of U1 small nuclear ribonucleoproteins (U1 snRNPs), suggesting that abnormalities in AS are partially mediated by changes in U1 snRNA levels. The shoot redifferentiation defectice2-1 (srd2-1) mutant defective for snRNA transcription was hypersensitive for stress treatment, since it showed changes in AS patterns at lower concentrations of stress inducers to compare with the wild type. Together, our data suggest that cellular stress can influence gene expression in plants by regulating AS, which is partially regulated by UsnRNA levels through the SRD2-mediated snRNA transcription.

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Journal
Plant Molecular Biology
Published
2025-03-16
DOI
https://doi.org/10.1007/s11103-025-01575-9
Primary Topic
RNA Research and Splicing
Type
article
Field-Weighted Citation Impact
0.00

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article

Chemically-induced cellular stress signals are transmitted to alternative splicing via UsnRNA levels to alter gene expression in Arabidopsis thaliana

Hirokazu Takahashi, Toshihiro Arae, Misato Ohtani, Taku Demura et al.
Plant Molecular Biology
RNA Research and Splicing
article

Chemically-induced cellular stress signals are transmitted to alternative splicing via UsnRNA levels to alter gene expression in Arabidopsis thaliana

Hirokazu Takahashi, Toshihiro Arae, Misato Ohtani, Taku Demura, Kohei Ishibashi, Ryosuke Sano
article en

Abstract

Alternative pre-mRNA splicing (AS) is a crucial regulatory layer of gene expression in eukaryotes. AS patterns can change in response to abiotic and biotic stress, allowing cellular functions to adapt to environmental conditions. Here, we examined the effects of cellular stress-inducing chemicals on AS-mediated gene regulation in Arabidopsis thaliana by investigating the alternatively spliced forms of SERINE-ARGININE PROTEIN30 (SRp30) and U1-70 K, encoding splicing factors, as well as ASCORBATE PEROXIDASE3 (APX3) and FOLYLPOLYGLUTAMATE SYNTHASE3 (FPGS3), encoding enzymes important for stress responses. Disrupting key cellular activities, including nitric oxide metabolism, ATPase activity, plastid function, and genome stability, affected AS patterns in Arabidopsis. Stress treatment altered the abundance of uridine-rich small nuclear RNAs (UsnRNAs), especially U1 snRNAs, which are essential non-coding RNA components of U1 small nuclear ribonucleoproteins (U1 snRNPs), suggesting that abnormalities in AS are partially mediated by changes in U1 snRNA levels. The shoot redifferentiation defectice2-1 (srd2-1) mutant defective for snRNA transcription was hypersensitive for stress treatment, since it showed changes in AS patterns at lower concentrations of stress inducers to compare with the wild type. Together, our data suggest that cellular stress can influence gene expression in plants by regulating AS, which is partially regulated by UsnRNA levels through the SRD2-mediated snRNA transcription.

Plant Molecular BiologyVol. 115(2)
RIKEN Center for Sustainable Resource Science (JP), The University of Tokyo (JP), Nara Institute of Science and Technology (JP)
Naito Foundation, Takeda Science Foundation, Sumitomo Foundation, Nara Institute of Science and Technology, Ministry of Education, Culture, Sports, Science and Technology, University of Tokyo, Toray Science Foundation, Japan Society for the Promotion of Science
Life in Land
Openalex Percentile: Top 96%
RNA Research and Splicing
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