Cited by 83RNA Research and SplicingPlant Molecular Biology ResearchPhotosynthetic Processes and Mechanisms

Tudor staphylococcal nuclease is a docking platform for stress granule components and is essential for SnRK1 activation in Arabidopsis

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Gutierrez‐Beltran, Emilio, Elander, Pernilla H, Dalman, Kerstin, Dayhoff, Guy W, Moschou, Panagiotis N, Uversky, Vladimir N, Crespo, Jose L, Bozhkov, Peter V·2021·The EMBO Journal

Published version of a preprint

Abstract

SUMMARY Adaptation to stress depends on the modulation of gene expression. Regulation of mRNA stability and degradation in stress granules (SGs), - cytoplasmic membraneless organelles composed of messenger ribonucleoprotein (mRNP) complexes, - plays an important role in fine-tuning of gene expression. In addition, SG formation can modulate stress signaling pathways by protein sequestration. Molecular composition, structure, and function of SGs in plants remain obscure. Recently, we established Tudor Staphylococcal Nuclease (TSN or Tudor-SN; also known as SND1) as integral component of SGs in Arabidopsis thaliana . Here, we combined purification of TSN interactome with cell biology, reverse genetics and bioinformatics to study composition and function of SGs in plants. We found that under both normal (in the absence of stress) and stress conditions TSN interactome is enriched in the homologues of known mammalian and yeast SG proteins, in addition to novel or plant-specific SG components. We estimate that upon stress perception, approximately half of TSN interactors are recruited to SGs de novo , in a stress-dependent manner, while another half represent a dense protein-protein interaction network pre-formed before onset of stress. Almost all TSN-interacting proteins are moderately or highly disordered and approximately 20% of them are predisposed for liquid-liquid phase separation (LLPS). This suggests that plant SGs, similarly to mammalian and yeast counterparts, are multicomponent viscous liquid droplets. Finally, we have discovered that evolutionary conserved SNF1-related protein kinase 1 (SnRK1) interacts with TSN in heat-induced SGs and that SnRK1 activation critically depends on the presence of TSN and formation of SGs. Altogether, our results establish TSN as a docking platform for SG-associated proteins and important stress signal mediator in plants.

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Authors
Gutierrez‐Beltran, E., Elander, P. H., Dalman, K., Dayhoff, G. W., Moschou, P. N., Uversky, V. N., Crespo, J. L., & Bozhkov, P. V.
Affiliations
  • Swedish University of Agricultural Sciences (SE)
  • University of South Florida (US)
  • University of Crete (GR)
  • Russian Academy of Sciences (RU)
Corresponding author
Bozhkov, Peter V
Venue
The EMBO Journal
Published
2021-07-21
Volume
40
Issue
17
Pages
e105043-e105043
ISSN
  • 0261-4189 (ISSN-L)
  • 1460-2075
OpenAlex
W3186280287
Cited by
83
References
131
Citations by year
2026: 11 · 2025: 11 · 2024: 24 · 2023: 17 · 2022: 15 · 2021: 5
FWCI
4.79
Type
journal article
Language
en
Open access
Locations
  • The EMBO Journal (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Epsilon Open Archive (Sveriges lantbruksuniversitet biblioteket (Swedish University of Agricultural Sciences)) (acceptedVersion)
  • Digital Commons - University of South Florida (University of South Florida) (submittedVersion, cc-by)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, other-oa)
  • Deposito de Investigacion Universidad de Sevilla (University of Seville) (submittedVersion, cc-by-nc-nd)
Funders
Universidad de Sevilla (PP2020/IV.4/029)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
Keywords
stress granules, SnRK1, AMPK, intrinsically disordered proteins, protein-protein interaction network, energy sensing, protein scaffolds, Arabidopsis thaliana, plant stress response
MeSH terms
Binding Sites, Cytoplasmic Granules, Protein Binding, Protein Serine-Threonine Kinases, Arabidopsis, Heat-Shock Response, Arabidopsis Proteins, Protein Interaction Maps, Intrinsically Disordered Proteins

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