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Mutation of Arabidopsis SME1 and Sm core assembly improves oxidative stress resilience

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Abstract
Alternative splicing is a key posttranscriptional gene regulatory process, acting in diverse adaptive and basal plant processes. Splicing of precursor-messenger RNA (pre-mRNA) is catalyzed by a dynamic ribonucleoprotein complex, designated the spliceosome. In a suppressor screen, we identified a nonsense mutation in the Smith (Sm) antigen protein SME1 to alleviate photorespiratory H2O2-dependent cell death in catalase deficient plants. Similar attenuation of cell death was observed upon chemical inhibition of the spliceosome, suggesting pre-mRNA splicing inhibition to be responsible for the observed cell death alleviation. Furthermore, the sme1-2 mutants showed increased tolerance to the reactive oxygen species inducing herbicide methyl viologen. Both an mRNA-seq and shotgun proteomic analysis in sme1-2 mutants displayed a constitutive molecular stress response, together with extensive alterations in pre-mRNA splicing of transcripts encoding metabolic enzymes and RNA binding proteins, even under unstressed conditions. Using SME1 as a bait to identify protein interactors, we provide experimental evidence for almost 50 homologs of the mammalian spliceosome-associated protein to reside in the Arabidopsis thaliana spliceosome complexes and propose roles in pre-mRNA splicing for four uncharacterized plant proteins. Furthermore, as for sme1-2, a mutant in the Sm core assembly protein ICLN resulted in a decreased sensitivity to methyl viologen. Taken together, these data show that both a perturbed Sm core composition and assembly results in the activation of a defense response and in enhanced resilience to oxidative stress.
Keywords
Physiology (medical), Biochemistry, Alternative splicing, Spliceosome, Sm protein, Oxidative stress, CATALASE2, Arabidopsis thaliana

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Citation

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MLA
Willems, Patrick, et al. “Mutation of Arabidopsis SME1 and Sm Core Assembly Improves Oxidative Stress Resilience.” FREE RADICAL BIOLOGY AND MEDICINE, vol. 200, 2023, pp. 117–29, doi:10.1016/j.freeradbiomed.2023.02.025.
APA
Willems, P., Van Ruyskensvelde, V., Maruta, T., Pottie, R., Fernández Fernández, Á. D., Pauwels, J., … Van Der Kelen, K. (2023). Mutation of Arabidopsis SME1 and Sm core assembly improves oxidative stress resilience. FREE RADICAL BIOLOGY AND MEDICINE, 200, 117–129. https://doi.org/10.1016/j.freeradbiomed.2023.02.025
Chicago author-date
Willems, Patrick, Valerie Van Ruyskensvelde, Takanori Maruta, Robin Pottie, Álvaro Daniel Fernández Fernández, Jarne Pauwels, Matthew A. Hannah, Kris Gevaert, Frank Van Breusegem, and Katrien Van Der Kelen. 2023. “Mutation of Arabidopsis SME1 and Sm Core Assembly Improves Oxidative Stress Resilience.” FREE RADICAL BIOLOGY AND MEDICINE 200: 117–29. https://doi.org/10.1016/j.freeradbiomed.2023.02.025.
Chicago author-date (all authors)
Willems, Patrick, Valerie Van Ruyskensvelde, Takanori Maruta, Robin Pottie, Álvaro Daniel Fernández Fernández, Jarne Pauwels, Matthew A. Hannah, Kris Gevaert, Frank Van Breusegem, and Katrien Van Der Kelen. 2023. “Mutation of Arabidopsis SME1 and Sm Core Assembly Improves Oxidative Stress Resilience.” FREE RADICAL BIOLOGY AND MEDICINE 200: 117–129. doi:10.1016/j.freeradbiomed.2023.02.025.
Vancouver
1.
Willems P, Van Ruyskensvelde V, Maruta T, Pottie R, Fernández Fernández ÁD, Pauwels J, et al. Mutation of Arabidopsis SME1 and Sm core assembly improves oxidative stress resilience. FREE RADICAL BIOLOGY AND MEDICINE. 2023;200:117–29.
IEEE
[1]
P. Willems et al., “Mutation of Arabidopsis SME1 and Sm core assembly improves oxidative stress resilience,” FREE RADICAL BIOLOGY AND MEDICINE, vol. 200, pp. 117–129, 2023.
@article{01GTVJ8PCTPZQ654S7BPPF6DCZ,
  abstract     = {{Alternative splicing is a key posttranscriptional gene regulatory process, acting in diverse adaptive and basal plant processes. Splicing of precursor-messenger RNA (pre-mRNA) is catalyzed by a dynamic ribonucleoprotein complex, designated the spliceosome. In a suppressor screen, we identified a nonsense mutation in the Smith (Sm) antigen protein SME1 to alleviate photorespiratory H2O2-dependent cell death in catalase deficient plants. Similar attenuation of cell death was observed upon chemical inhibition of the spliceosome, suggesting pre-mRNA splicing inhibition to be responsible for the observed cell death alleviation. Furthermore, the sme1-2 mutants showed increased tolerance to the reactive oxygen species inducing herbicide methyl viologen. Both an mRNA-seq and shotgun proteomic analysis in sme1-2 mutants displayed a constitutive molecular stress response, together with extensive alterations in pre-mRNA splicing of transcripts encoding metabolic enzymes and RNA binding proteins, even under unstressed conditions. Using SME1 as a bait to identify protein interactors, we provide experimental evidence for almost 50 homologs of the mammalian spliceosome-associated protein to reside in the Arabidopsis thaliana spliceosome complexes and propose roles in pre-mRNA splicing for four uncharacterized plant proteins. Furthermore, as for sme1-2, a mutant in the Sm core assembly protein ICLN resulted in a decreased sensitivity to methyl viologen. Taken together, these data show that both a perturbed Sm core composition and assembly results in the activation of a defense response and in enhanced resilience to oxidative stress.}},
  author       = {{Willems, Patrick and Van Ruyskensvelde, Valerie and Maruta, Takanori and Pottie, Robin and Fernández Fernández, Álvaro Daniel and Pauwels, Jarne and Hannah, Matthew A. and Gevaert, Kris and Van Breusegem, Frank and Van Der Kelen, Katrien}},
  issn         = {{0891-5849}},
  journal      = {{FREE RADICAL BIOLOGY AND MEDICINE}},
  keywords     = {{Physiology (medical),Biochemistry,Alternative splicing,Spliceosome,Sm protein,Oxidative stress,CATALASE2,Arabidopsis thaliana}},
  language     = {{eng}},
  pages        = {{117--129}},
  title        = {{Mutation of Arabidopsis SME1 and Sm core assembly improves oxidative stress resilience}},
  url          = {{http://doi.org/10.1016/j.freeradbiomed.2023.02.025}},
  volume       = {{200}},
  year         = {{2023}},
}

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