IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28414-5.html
   My bibliography  Save this article

Cotranslational N-degron masking by acetylation promotes proteome stability in plants

Author

Listed:
  • Eric Linster

    (Heidelberg University)

  • Francy L. Forero Ruiz

    (Heidelberg University)

  • Pavlina Miklankova

    (Heidelberg University)

  • Thomas Ruppert

    (Heidelberg University)

  • Johannes Mueller

    (Max-Planck-Institute for Biochemistry)

  • Laura Armbruster

    (Heidelberg University)

  • Xiaodi Gong

    (Heidelberg University)

  • Giovanna Serino

    (Sapienza Università di Roma)

  • Matthias Mann

    (Max-Planck-Institute for Biochemistry)

  • Rüdiger Hell

    (Heidelberg University)

  • Markus Wirtz

    (Heidelberg University)

Abstract

N-terminal protein acetylation (NTA) is a prevalent protein modification essential for viability in animals and plants. The dominant executor of NTA is the ribosome tethered Nα-acetyltransferase A (NatA) complex. However, the impact of NatA on protein fate is still enigmatic. Here, we demonstrate that depletion of NatA activity leads to a 4-fold increase in global protein turnover via the ubiquitin-proteasome system in Arabidopsis. Surprisingly, a concomitant increase in translation, actioned via enhanced Target-of-Rapamycin activity, is also observed, implying that defective NTA triggers feedback mechanisms to maintain steady-state protein abundance. Quantitative analysis of the proteome, the translatome, and the ubiquitome reveals that NatA substrates account for the bulk of this enhanced turnover. A targeted analysis of NatA substrate stability uncovers that NTA absence triggers protein destabilization via a previously undescribed and widely conserved nonAc/N-degron in plants. Hence, the imprinting of the proteome with acetylation marks is essential for coordinating proteome stability.

Suggested Citation

  • Eric Linster & Francy L. Forero Ruiz & Pavlina Miklankova & Thomas Ruppert & Johannes Mueller & Laura Armbruster & Xiaodi Gong & Giovanna Serino & Matthias Mann & Rüdiger Hell & Markus Wirtz, 2022. "Cotranslational N-degron masking by acetylation promotes proteome stability in plants," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28414-5
    DOI: 10.1038/s41467-022-28414-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28414-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28414-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Daniel J. Gibbs & Seung Cho Lee & Nurulhikma Md Isa & Silvia Gramuglia & Takeshi Fukao & George W. Bassel & Cristina Sousa Correia & Françoise Corbineau & Frederica L. Theodoulou & Julia Bailey-Serres, 2011. "Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants," Nature, Nature, vol. 479(7373), pages 415-418, November.
    2. Felix Alexander Weyer & Andrea Gumiero & Karine Lapouge & Gert Bange & Jürgen Kopp & Irmgard Sinning, 2017. "Structural basis of HypK regulating N-terminal acetylation by the NatA complex," Nature Communications, Nature, vol. 8(1), pages 1-10, August.
    3. Eric Linster & Iwona Stephan & Willy V. Bienvenut & Jodi Maple-Grødem & Line M. Myklebust & Monika Huber & Michael Reichelt & Carsten Sticht & Simon Geir Møller & Thierry Meinnel & Thomas Arnesen & Ca, 2015. "Downregulation of N-terminal acetylation triggers ABA-mediated drought responses in Arabidopsis," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    4. Yihan Dong & Marleen Silbermann & Anna Speiser & Ilaria Forieri & Eric Linster & Gernot Poschet & Arman Allboje Samami & Mutsumi Wanatabe & Carsten Sticht & Aurelio A. Teleman & Jean-Marc Deragon & Ka, 2017. "RETRACTED ARTICLE: Sulfur availability regulates plant growth via glucose-TOR signaling," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Yao Li & Yueling Zhao & Xiaojie Yan & Chen Ye & Sara Weirich & Bing Zhang & Xiaolu Wang & Lili Song & Chenhao Jiang & Albert Jeltsch & Cheng Dong & Wenyi Mi, 2022. "CRL2ZER1/ZYG11B recognizes small N-terminal residues for degradation," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Sylvia Varland & Rui Duarte Silva & Ine Kjosås & Alexandra Faustino & Annelies Bogaert & Maximilian Billmann & Hadi Boukhatmi & Barbara Kellen & Michael Costanzo & Adrian Drazic & Camilla Osberg & Kat, 2023. "N-terminal acetylation shields proteins from degradation and promotes age-dependent motility and longevity," Nature Communications, Nature, vol. 14(1), pages 1-27, December.
    3. Charlotte M. François & Thomas Pihl & Marion Dunoyer de Segonzac & Chloé Hérault & Bruno Hudry, 2023. "Metabolic regulation of proteome stability via N-terminal acetylation controls male germline stem cell differentiation and reproduction," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Viorica Chelban & Henriette Aksnes & Reza Maroofian & Lauren C. LaMonica & Luis Seabra & Anette Siggervåg & Perrine Devic & Hanan E. Shamseldin & Jana Vandrovcova & David Murphy & Anne-Claire Richard , 2024. "Biallelic NAA60 variants with impaired N-terminal acetylation capacity cause autosomal recessive primary familial brain calcifications," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. Hongliang Zhang & Julia Quintana & Koray Ütkür & Lorenz Adrian & Harmen Hawer & Klaus Mayer & Xiaodi Gong & Leonardo Castanedo & Anna Schulten & Nadežda Janina & Marcus Peters & Markus Wirtz & Ulrich , 2022. "Translational fidelity and growth of Arabidopsis require stress-sensitive diphthamide biosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Ulises H. Guzman & Henriette Aksnes & Rasmus Ree & Nicolai Krogh & Magnus E. Jakobsson & Lars J. Jensen & Thomas Arnesen & Jesper V. Olsen, 2023. "Loss of N-terminal acetyltransferase A activity induces thermally unstable ribosomal proteins and increases their turnover in Saccharomyces cerevisiae," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Charlotte M. François & Thomas Pihl & Marion Dunoyer de Segonzac & Chloé Hérault & Bruno Hudry, 2023. "Metabolic regulation of proteome stability via N-terminal acetylation controls male germline stem cell differentiation and reproduction," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Verna Van & Janae B. Brown & Corin R. O’Shea & Hannah Rosenbach & Ijaz Mohamed & Nna-Emeka Ejimogu & Toan S. Bui & Veronika A. Szalai & Kelly N. Chacón & Ingrid Span & Fangliang Zhang & Aaron T. Smith, 2023. "Iron-sulfur clusters are involved in post-translational arginylation," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Agata Zubrycka & Charlene Dambire & Laura Dalle Carbonare & Gunjan Sharma & Tinne Boeckx & Kamal Swarup & Craig J. Sturrock & Brian S. Atkinson & Ranjan Swarup & Françoise Corbineau & Neil J. Oldham &, 2023. "ERFVII action and modulation through oxygen-sensing in Arabidopsis thaliana," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Ulises H. Guzman & Henriette Aksnes & Rasmus Ree & Nicolai Krogh & Magnus E. Jakobsson & Lars J. Jensen & Thomas Arnesen & Jesper V. Olsen, 2023. "Loss of N-terminal acetyltransferase A activity induces thermally unstable ribosomal proteins and increases their turnover in Saccharomyces cerevisiae," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28414-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.