Reticulon proteins modulate autophagy of the endoplasmic reticulum in maize endosperm

  1. Xiaoguo Zhang
  2. Xinxin Ding
  3. Richard Scott Marshall
  4. Julio Paez-Valencia
  5. Patrick Lacey
  6. Richard David Vierstra
  7. Marisa Otegui  Is a corresponding author
  1. University of Wisconsin-Madison, United States
  2. Washington University in St Louis, United States

Abstract

Reticulon (Rtn) proteins shape tubular domains of the endoplasmic reticulum (ER), and in some cases are autophagy receptors for selective ER turnover. We have found that maize Rtn1 and Rtn2 control ER homeostasis and autophagic flux in endosperm aleurone cells, where the ER accumulates lipid droplets and synthesizes storage protein accretions metabolized during germination. Maize Rtn1 and Rtn2 are expressed in the endosperm, localize to the ER, and re-model ER architecture in a dose-dependent manner. Rtn1 and Rtn2 interact with Atg8a using four Atg8-interacting motifs (AIMs) located at the C-terminus, cytoplasmic loop, and within the transmembrane segments. Binding between Rtn2 and Atg8 is elevated upon ER stress. Maize rtn2 mutants display increased autophagy and up-regulation of an ER stress-responsive chaperone. We propose that maize Rtn1 and Rtn2 act as receptors for autophagy-mediated ER turnover, and thus are critical for ER homeostasis and suppression of ER stress.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

The following previously published data sets were used

Article and author information

Author details

  1. Xiaoguo Zhang

    Department of Botany, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Xinxin Ding

    Department of Botany, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Richard Scott Marshall

    Department of Biology, Washington University in St Louis, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6844-1078
  4. Julio Paez-Valencia

    Department of Botany, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Patrick Lacey

    Department of Botany, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Richard David Vierstra

    Department of Biology, Washington University in St Louis, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0210-3516
  7. Marisa Otegui

    Department of Botany, University of Wisconsin-Madison, Madison, United States
    For correspondence
    otegui@wisc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4699-6950

Funding

National Science Foundation (IOS-1840687)

  • Marisa Otegui

Agriculture Hatch Act Formula Fund (WIS01791)

  • Marisa Otegui

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Dominique C Bergmann, Stanford University, United States

Publication history

  1. Received: September 16, 2019
  2. Accepted: February 2, 2020
  3. Accepted Manuscript published: February 3, 2020 (version 1)
  4. Version of Record published: February 27, 2020 (version 2)

Copyright

© 2020, Zhang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Xiaoguo Zhang
  2. Xinxin Ding
  3. Richard Scott Marshall
  4. Julio Paez-Valencia
  5. Patrick Lacey
  6. Richard David Vierstra
  7. Marisa Otegui
(2020)
Reticulon proteins modulate autophagy of the endoplasmic reticulum in maize endosperm
eLife 9:e51918.
https://doi.org/10.7554/eLife.51918

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