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Pexophagy suppresses ROS-induced damage in leaf cells under high-intensity light

Author

Listed:
  • Kazusato Oikawa

    (National Institute for Basic Biology
    Kyoto University, Katsura)

  • Shino Goto-Yamada

    (Jagiellonian University)

  • Yasuko Hayashi

    (Niigata University)

  • Daisuke Takahashi

    (Iwate University
    Saitama University)

  • Yoshitaka Kimori

    (National Institutes of Natural Sciences
    National Institute for Basic Biology
    Fukui University of Technology)

  • Michitaro Shibata

    (RIKEN Center for Sustainable Resource Science)

  • Kohki Yoshimoto

    (School of Agriculture)

  • Atsushi Takemiya

    (Yamaguchi University)

  • Maki Kondo

    (National Institute for Basic Biology)

  • Kazumi Hikino

    (National Institute for Basic Biology)

  • Akira Kato

    (Niigata University)

  • Keisuke Shimoda

    (Niigata University)

  • Haruko Ueda

    (Konan University)

  • Matsuo Uemura

    (Iwate University
    Iwate University)

  • Keiji Numata

    (RIKEN Center for Sustainable Resource Science
    Kyoto University, Katsura)

  • Yoshinori Ohsumi

    (Tokyo Institute of Technology)

  • Ikuko Hara-Nishimura

    (Konan University)

  • Shoji Mano

    (National Institute for Basic Biology
    SOKENDAI (The Graduate University for Advanced Studies))

  • Kenji Yamada

    (Jagiellonian University)

  • Mikio Nishimura

    (National Institute for Basic Biology
    Konan University)

Abstract

Although light is essential for photosynthesis, it has the potential to elevate intracellular levels of reactive oxygen species (ROS). Since high ROS levels are cytotoxic, plants must alleviate such damage. However, the cellular mechanism underlying ROS-induced leaf damage alleviation in peroxisomes was not fully explored. Here, we show that autophagy plays a pivotal role in the selective removal of ROS-generating peroxisomes, which protects plants from oxidative damage during photosynthesis. We present evidence that autophagy-deficient mutants show light intensity-dependent leaf damage and excess aggregation of ROS-accumulating peroxisomes. The peroxisome aggregates are specifically engulfed by pre-autophagosomal structures and vacuolar membranes in both leaf cells and isolated vacuoles, but they are not degraded in mutants. ATG18a-GFP and GFP-2×FYVE, which bind to phosphatidylinositol 3-phosphate, preferentially target the peroxisomal membranes and pre-autophagosomal structures near peroxisomes in ROS-accumulating cells under high-intensity light. Our findings provide deeper insights into the plant stress response caused by light irradiation.

Suggested Citation

  • Kazusato Oikawa & Shino Goto-Yamada & Yasuko Hayashi & Daisuke Takahashi & Yoshitaka Kimori & Michitaro Shibata & Kohki Yoshimoto & Atsushi Takemiya & Maki Kondo & Kazumi Hikino & Akira Kato & Keisuke, 2022. "Pexophagy suppresses ROS-induced damage in leaf cells under high-intensity light," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35138-z
    DOI: 10.1038/s41467-022-35138-z
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    References listed on IDEAS

    as
    1. Noboru Mizushima & Takeshi Noda & Tamotsu Yoshimori & Yae Tanaka & Tomoko Ishii & Michael D. George & Daniel J. Klionsky & Mariko Ohsumi & Yoshinori Ohsumi, 1998. "A protein conjugation system essential for autophagy," Nature, Nature, vol. 395(6700), pages 395-398, September.
    2. Jinglei Cheng & Akikazu Fujita & Hayashi Yamamoto & Tsuyako Tatematsu & Soichiro Kakuta & Keisuke Obara & Yoshinori Ohsumi & Toyoshi Fujimoto, 2014. "Yeast and mammalian autophagosomes exhibit distinct phosphatidylinositol 3-phosphate asymmetries," Nature Communications, Nature, vol. 5(1), pages 1-12, May.
    3. Jinglei Cheng & Akikazu Fujita & Hayashi Yamamoto & Tsuyako Tatematsu & Soichiro Kakuta & Keisuke Obara & Yoshinori Ohsumi & Toyoshi Fujimoto, 2014. "Erratum: Yeast and mammalian autophagosomes exhibit distinct phosphatidylinositol 3-phosphate asymmetries," Nature Communications, Nature, vol. 5(1), pages 1-2, December.
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