Selective autophagy regulates chloroplast protein import and promotes plant stress tolerance

Chloroplasts are plant organelles responsible for photosynthesis and environmental sensing. Most chloroplast proteins are imported from the cytosol through the translocon at the outer envelope membrane of chloroplasts (TOC). Previous work has shown that TOC components are regulated by the ubiquitin‐...

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Veröffentlicht in:The EMBO journal 2023-07, Vol.42 (14), p.e112534-n/a
Hauptverfasser: Wan, Chen, Zhang, Hui, Cheng, Hongying, Sowden, Robert G, Cai, Wenjuan, Jarvis, R Paul, Ling, Qihua
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Sprache:eng
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Zusammenfassung:Chloroplasts are plant organelles responsible for photosynthesis and environmental sensing. Most chloroplast proteins are imported from the cytosol through the translocon at the outer envelope membrane of chloroplasts (TOC). Previous work has shown that TOC components are regulated by the ubiquitin‐proteasome system (UPS) to control the chloroplast proteome, which is crucial for the organelle's function and plant development. Here, we demonstrate that the TOC apparatus is also subject to K63‐linked polyubiquitination and regulation by selective autophagy, potentially promoting plant stress tolerance. We identify NBR1 as a selective autophagy adaptor targeting TOC components, and mediating their relocation into vacuoles for autophagic degradation. Such selective autophagy is shown to control TOC protein levels and chloroplast protein import and to influence photosynthetic activity as well as tolerance to UV‐B irradiation and heat stress in Arabidopsis plants. These findings uncover the vital role of selective autophagy in the proteolytic regulation of specific chloroplast proteins, and how dynamic control of chloroplast protein import is critically important for plants to cope with challenging environments. Synopsis Chloroplasts regulate their proteome in response to stress by degrading specific proteins via proteases and the ubiquitin‐proteasome system. This work reveals an additional involvement of the autophagy adaptor NBR1, mediating autophagic turnover of specific chloroplast proteins and optimizes plant stress tolerance. Chloroplast protein import apparatus (TOC) components are degraded by selective autophagy. NBR1 recruits ATG8 to ubiquitinated TOC protein cargos, promoting their autophagic degradation. Plants respond to UVB and heat stress by regulating chloroplast protein import and photosynthetic capacity. Graphical Abstract Heat and UV light stress promotes the NBR1‐mediated autophagy of specific chloroplast import apparatus components in Arabidopsis .
ISSN:0261-4189
1460-2075
DOI:10.15252/embj.2022112534