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Plant AtEH/Pan1 proteins drive autophagosome formation at ER-PM contact sites with actin and endocytic machinery

Author

Listed:
  • Pengwei Wang

    (Durham University
    Huazhong Agricultural University)

  • Roman Pleskot

    (Ghent University
    VIB Center for Plant Systems Biology)

  • Jingze Zang

    (Durham University
    Huazhong Agricultural University)

  • Joanna Winkler

    (Ghent University
    VIB Center for Plant Systems Biology)

  • Jie Wang

    (Ghent University)

  • Klaas Yperman

    (Ghent University
    VIB Center for Plant Systems Biology)

  • Tong Zhang

    (Huazhong Agricultural University)

  • Kun Wang

    (Huazhong Agricultural University)

  • Jinli Gong

    (Huazhong Agricultural University)

  • Yajie Guan

    (Huazhong Agricultural University)

  • Christine Richardson

    (Durham University)

  • Patrick Duckney

    (Durham University)

  • Michael Vandorpe

    (Ghent University
    VIB Center for Plant Systems Biology)

  • Evelien Mylle

    (Ghent University
    VIB Center for Plant Systems Biology)

  • Jindriska Fiserova

    (Durham University
    Institute of Molecular Genetics CAS)

  • Daniel Van Damme

    (Ghent University
    VIB Center for Plant Systems Biology)

  • Patrick J. Hussey

    (Durham University)

Abstract

The Arabidopsis EH proteins (AtEH1/Pan1 and AtEH2/Pan1) are components of the endocytic TPLATE complex (TPC) which is essential for endocytosis. Both proteins are homologues of the yeast ARP2/3 complex activator, Pan1p. Here, we show that these proteins are also involved in actin cytoskeleton regulated autophagy. Both AtEH/Pan1 proteins localise to the plasma membrane and autophagosomes. Upon induction of autophagy, AtEH/Pan1 proteins recruit TPC and AP-2 subunits, clathrin, actin and ARP2/3 proteins to autophagosomes. Increased expression of AtEH/Pan1 proteins boosts autophagosome formation, suggesting independent and redundant pathways for actin-mediated autophagy in plants. Moreover, AtEHs/Pan1-regulated autophagosomes associate with ER-PM contact sites (EPCS) where AtEH1/Pan1 interacts with VAP27-1. Knock-down expression of either AtEH1/Pan1 or VAP27-1 makes plants more susceptible to nutrient depleted conditions, indicating that the autophagy pathway is perturbed. In conclusion, we identify the existence of an autophagy-dependent pathway in plants to degrade endocytic components, starting at the EPCS through the interaction among AtEH/Pan1, actin cytoskeleton and the EPCS resident protein VAP27-1.

Suggested Citation

  • Pengwei Wang & Roman Pleskot & Jingze Zang & Joanna Winkler & Jie Wang & Klaas Yperman & Tong Zhang & Kun Wang & Jinli Gong & Yajie Guan & Christine Richardson & Patrick Duckney & Michael Vandorpe & E, 2019. "Plant AtEH/Pan1 proteins drive autophagosome formation at ER-PM contact sites with actin and endocytic machinery," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12782-6
    DOI: 10.1038/s41467-019-12782-6
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    Cited by:

    1. Rodrigo Enrique Gomez & Clément Chambaud & Josselin Lupette & Julie Castets & Stéphanie Pascal & Lysiane Brocard & Lise Noack & Yvon Jaillais & Jérôme Joubès & Amélie Bernard, 2022. "Phosphatidylinositol-4-phosphate controls autophagosome formation in Arabidopsis thaliana," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Lin-lin Zhao & Ru Chen & Ziyu Bai & Junyi Liu & Yuhao Zhang & Yicheng Zhong & Meng-xiang Sun & Peng Zhao, 2024. "Autophagy-mediated degradation of integumentary tapetum is critical for embryo pattern formation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Chengyang Li & Patrick Duckney & Tong Zhang & Yanshu Fu & Xin Li & Johan Kroon & Geert Jaeger & Yunjiang Cheng & Patrick J. Hussey & Pengwei Wang, 2022. "TraB family proteins are components of ER-mitochondrial contact sites and regulate ER-mitochondrial interactions and mitophagy," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Luciana Renna & Giovanni Stefano & Maria Paola Puggioni & Sang-Jin Kim & Anastasiya Lavell & John E. Froehlich & Graham Burkart & Stefano Mancuso & Christoph Benning & Federica Brandizzi, 2024. "ER-associated VAP27-1 and VAP27-3 proteins functionally link the lipid-binding ORP2A at the ER-chloroplast contact sites," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Timothy J. Hawkins & Michaela Kopischke & Patrick J. Duckney & Katarzyna Rybak & David A. Mentlak & Johan T. M. Kroon & Mai Thu Bui & A. Christine Richardson & Mary Casey & Agnieszka Alexander & Geert, 2023. "NET4 and RabG3 link actin to the tonoplast and facilitate cytoskeletal remodelling during stomatal immunity," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. José Cerca & Bent Petersen & José Miguel Lazaro-Guevara & Angel Rivera-Colón & Siri Birkeland & Joel Vizueta & Siyu Li & Qionghou Li & João Loureiro & Chatchai Kosawang & Patricia Jaramillo Díaz & Gon, 2022. "The genomic basis of the plant island syndrome in Darwin’s giant daisies," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. Tong Zhang & Yifan Li & Chengyang Li & Jingze Zang & Erlin Gao & Johan T. Kroon & Xiaolu Qu & Patrick J. Hussey & Pengwei Wang, 2023. "Exo84c interacts with VAP27 to regulate exocytotic compartment degradation and stigma senescence," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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