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Tudor Staphylococcal Nuclease Links Formation of Stress Granules and Processing Bodies with mRNA Catabolism in Arabidopsis

Emilio Gutierrez-Beltran, Panagiotis N. Moschou, Andrei P. Smertenko, Peter V. Bozhkov
Emilio Gutierrez-Beltran
Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, SE-75007 Uppsala, Sweden
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Panagiotis N. Moschou
Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, SE-75007 Uppsala, Sweden
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  • For correspondence: panagiotis.moschou@slu.se
Andrei P. Smertenko
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164Institute for Global Food Security, Queen’s University Belfast, Belfast BT9 5BN, United Kingdom
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Peter V. Bozhkov
Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, SE-75007 Uppsala, Sweden
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Published March 2015. DOI: https://doi.org/10.1105/tpc.114.134494

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  • © 2015 American Society of Plant Biologists. All rights reserved.

Abstract

Tudor Staphylococcal Nuclease (TSN or Tudor-SN; also known as SND1) is an evolutionarily conserved protein involved in the transcriptional and posttranscriptional regulation of gene expression in animals. Although TSN was found to be indispensable for normal plant development and stress tolerance, the molecular mechanisms underlying these functions remain elusive. Here, we show that Arabidopsis thaliana TSN is essential for the integrity and function of cytoplasmic messenger ribonucleoprotein (mRNP) complexes called stress granules (SGs) and processing bodies (PBs), sites of posttranscriptional gene regulation during stress. TSN associates with SGs following their microtubule-dependent assembly and plays a scaffolding role in both SGs and PBs. The enzymatically active tandem repeat of four SN domains is crucial for targeting TSN to the cytoplasmic mRNA complexes and is sufficient for the cytoprotective function of TSN during stress. Furthermore, our work connects the cytoprotective function of TSN with its positive role in stress-induced mRNA decapping. While stress led to a pronounced increase in the accumulation of uncapped mRNAs in wild-type plants, this increase was abrogated in TSN knockout plants. Taken together, our results establish TSN as a key enzymatic component of the catabolic machinery responsible for the processing of mRNAs in the cytoplasmic mRNP complexes during stress.

  • Glossary

    SG
    stress granule
    PB
    processing body
    MT
    microtubule
    CHX
    cycloheximide
    APM
    amiprophos-methyl
    FRAP
    fluorescence recovery after photobleaching
    Ler
    Landsberg erecta
    Col
    Columbia-0
    pdTp
    3′,5′-deoxythymidine bisphosphate
    dTp
    3′-deoxythymidine monophosphate
    FDA
    fluorescein diacetate
    mRNP
    messenger ribonucleoprotein
    GO
    Gene Ontology
    MS
    Murashige and Skoog
    PBST
    PBS buffer supplemented with Tween 20
    dsDNA
    double-stranded DNA
    cRNA
    copy RNA
    LMS
    liquid MS medium
    • Received November 25, 2014.
    • Revised February 3, 2015.
    • Accepted February 16, 2015.
    • Published March 3, 2015.
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    Tudor Staphylococcal Nuclease Links Formation of Stress Granules and Processing Bodies with mRNA Catabolism in Arabidopsis
    Emilio Gutierrez-Beltran, Panagiotis N. Moschou, Andrei P. Smertenko, Peter V. Bozhkov
    The Plant Cell Mar 2015, 27 (3) 926-943; DOI: 10.1105/tpc.114.134494

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    Tudor Staphylococcal Nuclease Links Formation of Stress Granules and Processing Bodies with mRNA Catabolism in Arabidopsis
    Emilio Gutierrez-Beltran, Panagiotis N. Moschou, Andrei P. Smertenko, Peter V. Bozhkov
    The Plant Cell Mar 2015, 27 (3) 926-943; DOI: 10.1105/tpc.114.134494
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    The Plant Cell: 27 (3)
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