The autophagy receptor NBR1 directs the clearance of photodamaged chloroplasts
- University of Wisconsin-Madison, United States
- Washington University in St. Louis, United States
- Universidad de la República, Uruguay
- University of Western Australia, Australia
Abstract
The ubiquitin-binding NBR1 autophagy receptor plays a prominent role in recognizing ubiquitylated protein aggregates for vacuolar degradation by macroautophagy. Here, we show that upon exposing Arabidopsis plants to intense light, NBR1 associates with photodamaged chloroplasts independently of ATG7, a core component of the canonical autophagy machinery. NBR1 coats both the surface and interior of chloroplasts, which is then followed by direct engulfment of the organelles into the central vacuole via a microautophagy-type process. The relocalization of NBR1 into chloroplasts does not require the chloroplast translocon complexes embedded in the envelope but is instead greatly enhanced by removing the self-oligomerization mPB1 domain of NBR1. The delivery of NBR1-decorated chloroplasts into vacuoles depends on the ubiquitin-binding UBA2 domain of NBR1 but is independent of the ubiquitin E3 ligases SP1 and PUB4, known to direct the ubiquitylation of chloroplast surface proteins. Compared to wild-type plants, nbr1 mutants have altered levels of a subset of chloroplast proteins and display abnormal chloroplast density and sizes upon high light exposure. We postulate that, as photodamaged chloroplasts lose envelope integrity, cytosolic ligases reach the chloroplast interior to ubiquitylate thylakoid and stroma proteins which are then recognized by NBR1 for autophagic clearance. This study uncovers a new function of NBR1 in the degradation of damaged chloroplasts by microautophagy.
Data availability
The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD039183. All other data generated or analyzed during this study are included in the manuscript and supporting file
Article and author information
Author details
Richard David Vierstra
Funding
National Science Foundation (IOS-1840687)
- Marisa S Otegui
U.S. Department of Energy (DE-SC0019013)
- Marisa S Otegui
National Institutes of Health (1S10 OD026769-01)
- Marisa S Otegui
National Institutes of Health (R01-GM124452)
- Richard David Vierstra
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, Lee 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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The autophagy receptor NBR1 directs the clearance of photodamaged chloroplasts
eLife 12:e86030.
https://doi.org/10.7554/eLife.86030
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