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ER-associated VAP27-1 and VAP27-3 proteins functionally link the lipid-binding ORP2A at the ER-chloroplast contact sites

Author

Listed:
  • Luciana Renna

    (Michigan State University
    University of Florence)

  • Giovanni Stefano

    (Michigan State University
    Michigan State University
    University of Florence)

  • Maria Paola Puggioni

    (Michigan State University
    Umeå University)

  • Sang-Jin Kim

    (Michigan State University
    Michigan State University
    Michigan State University)

  • Anastasiya Lavell

    (Michigan State University)

  • John E. Froehlich

    (Michigan State University
    Michigan State University)

  • Graham Burkart

    (Michigan State University)

  • Stefano Mancuso

    (University of Florence
    Fondazione per il Futuro delle Città)

  • Christoph Benning

    (Michigan State University
    Michigan State University
    Michigan State University)

  • Federica Brandizzi

    (Michigan State University
    Michigan State University
    Michigan State University)

Abstract

The plant endoplasmic reticulum (ER) contacts heterotypic membranes at membrane contact sites (MCSs) through largely undefined mechanisms. For instance, despite the well-established and essential role of the plant ER-chloroplast interactions for lipid biosynthesis, and the reported existence of physical contacts between these organelles, almost nothing is known about the ER-chloroplast MCS identity. Here we show that the Arabidopsis ER membrane-associated VAP27 proteins and the lipid-binding protein ORP2A define a functional complex at the ER-chloroplast MCSs. Specifically, through in vivo and in vitro association assays, we found that VAP27 proteins interact with the outer envelope membrane (OEM) of chloroplasts, where they bind to ORP2A. Through lipidomic analyses, we established that VAP27 proteins and ORP2A directly interact with the chloroplast OEM monogalactosyldiacylglycerol (MGDG), and we demonstrated that the loss of the VAP27-ORP2A complex is accompanied by subtle changes in the acyl composition of MGDG and PG. We also found that ORP2A interacts with phytosterols and established that the loss of the VAP27-ORP2A complex alters sterol levels in chloroplasts. We propose that, by interacting directly with OEM lipids, the VAP27-ORP2A complex defines plant-unique MCSs that bridge ER and chloroplasts and are involved in chloroplast lipid homeostasis.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50425-7
    DOI: 10.1038/s41467-024-50425-7
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    References listed on IDEAS

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    1. 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.
    2. 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.
    3. Camilla Raiborg & Eva M. Wenzel & Nina M. Pedersen & Hallvard Olsvik & Kay O. Schink & Sebastian W. Schultz & Marina Vietri & Veronica Nisi & Cecilia Bucci & Andreas Brech & Terje Johansen & Harald St, 2015. "Repeated ER–endosome contacts promote endosome translocation and neurite outgrowth," Nature, Nature, vol. 520(7546), pages 234-238, April.
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