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.

Pexophagy plays a pivotal role in the selective removal of ROS-generating peroxisomes, which protects plants from oxidative damage during photosynthesis under high-intensity light.

Details

Title
Pexophagy suppresses ROS-induced damage in leaf cells under high-intensity light
Author
Oikawa, Kazusato 1   VIAFID ORCID Logo  ; Goto-Yamada, Shino 2 ; Hayashi, Yasuko 3 ; Takahashi, Daisuke 4   VIAFID ORCID Logo  ; Kimori, Yoshitaka 5 ; Shibata, Michitaro 6 ; Yoshimoto, Kohki 7 ; Takemiya, Atsushi 8   VIAFID ORCID Logo  ; Kondo, Maki 9 ; Hikino, Kazumi 10 ; Kato, Akira 3 ; Shimoda, Keisuke 3 ; Ueda, Haruko 11 ; Uemura, Matsuo 12   VIAFID ORCID Logo  ; Numata, Keiji 13 ; Ohsumi, Yoshinori 14   VIAFID ORCID Logo  ; Hara-Nishimura, Ikuko 11   VIAFID ORCID Logo  ; Mano, Shoji 15 ; Yamada, Kenji 2   VIAFID ORCID Logo  ; Nishimura, Mikio 16   VIAFID ORCID Logo 

1  National Institute for Basic Biology, Department of Cell Biology, Okazaki, Japan (GRID:grid.419396.0) (ISNI:0000 0004 0618 8593); Kyoto University, Katsura, Kyoto, Japan (GRID:grid.258799.8) (ISNI:0000 0004 0372 2033) 
2  Jagiellonian University, Malopolska Centre of Biotechnology, Krakow, Poland (GRID:grid.5522.0) (ISNI:0000 0001 2162 9631) 
3  Niigata University, Department of Science, Faculty of Science, Niigata, Japan (GRID:grid.260975.f) (ISNI:0000 0001 0671 5144) 
4  Iwate University, United Graduate School of Agricultural Sciences, Iwate, Japan (GRID:grid.411792.8) (ISNI:0000 0001 0018 0409); Saitama University, Graduate School of Science and Engineering, Saitama, Japan (GRID:grid.263023.6) (ISNI:0000 0001 0703 3735) 
5  National Institutes of Natural Sciences, Department of Imaging Science, Center for Novel Science Initiatives, Okazaki, Japan (GRID:grid.250358.9) (ISNI:0000 0000 9137 6732); National Institute for Basic Biology, Laboratory of Biological Diversity, Department of Evolutionary and Biodiversity, Okazaki, Japan (GRID:grid.419396.0) (ISNI:0000 0004 0618 8593); Fukui University of Technology, Department of Management and Information Sciences, Faculty of Environmental and Information Sciences, Fukui, Japan (GRID:grid.440871.e) (ISNI:0000 0000 9829 078X) 
6  RIKEN Center for Sustainable Resource Science, Yokohama, Japan (GRID:grid.509461.f) (ISNI:0000 0004 1757 8255) 
7  School of Agriculture, Department of Life Sciences, Meiji University, Japan (GRID:grid.411764.1) (ISNI:0000 0001 2106 7990) 
8  Yamaguchi University, Department of Biology, Graduate School of Sciences and Technology for Innovation, Yamaguchi, Japan (GRID:grid.268397.1) (ISNI:0000 0001 0660 7960) 
9  National Institute for Basic Biology, Department of Cell Biology, Okazaki, Japan (GRID:grid.419396.0) (ISNI:0000 0004 0618 8593) 
10  National Institute for Basic Biology, Laboratory of Organelle Regulation, Okazaki, Japan (GRID:grid.419396.0) (ISNI:0000 0004 0618 8593) 
11  Konan University, Faculty of Science and Engineering, Kobe, Japan (GRID:grid.258669.6) (ISNI:0000 0000 8565 5938) 
12  Iwate University, United Graduate School of Agricultural Sciences, Iwate, Japan (GRID:grid.411792.8) (ISNI:0000 0001 0018 0409); Iwate University, Department of Plant-bioscience, Morioka, Japan (GRID:grid.411792.8) (ISNI:0000 0001 0018 0409) 
13  RIKEN Center for Sustainable Resource Science, Biomacromolecules Research Team, Wako, Japan (GRID:grid.509461.f) (ISNI:0000 0004 1757 8255); Kyoto University, Katsura, Kyoto, Japan (GRID:grid.258799.8) (ISNI:0000 0004 0372 2033) 
14  Tokyo Institute of Technology, Cell Biology Center, Institute of Innovative Research, Yokohama, Japan (GRID:grid.32197.3e) (ISNI:0000 0001 2179 2105) 
15  National Institute for Basic Biology, Laboratory of Organelle Regulation, Okazaki, Japan (GRID:grid.419396.0) (ISNI:0000 0004 0618 8593); SOKENDAI (The Graduate University for Advanced Studies), Department of Basic Biology, School of Life Science, Okazaki, Japan (GRID:grid.275033.0) (ISNI:0000 0004 1763 208X) 
16  National Institute for Basic Biology, Department of Cell Biology, Okazaki, Japan (GRID:grid.419396.0) (ISNI:0000 0004 0618 8593); Konan University, Faculty of Science and Engineering, Kobe, Japan (GRID:grid.258669.6) (ISNI:0000 0000 8565 5938) 
Publication year
2022
Publication date
2022
Publisher
Nature Publishing Group
e-ISSN
20411723
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.1038/s41467-022-35138-z
ProQuest document ID
2746829767
Copyright
© The Author(s) 2022. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.