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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
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    References listed on IDEAS

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    1. 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.
    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. 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.
    4. 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.
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    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. Karen C. Heathcote & Thomas P. Keeley & Matti Myllykoski & Malin Lundekvam & Nina McTiernan & Salma Akter & Norma Masson & Peter J. Ratcliffe & Thomas Arnesen & Emily Flashman, 2024. "N-terminal cysteine acetylation and oxidation patterns may define protein stability," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. 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.
    7. 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.

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