Selective autophagy regulates chloroplast protein import and promotes plant stress tolerance

Abstract

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.

Dynamic protein-protein interactions of the potato autophagy-related StATG8 family proteins, which are also associated with WRKY transcription factor and pathogen effector in the nucleus

“…NBR1 (Next to BRCA1 gene 1), are responsible for autophagic degradation of ubiquitinated NBR1 targets cargo and physically interacts with the ATG8 protein to promote cargo envelopment into autophagosomes [32]. NBR1 protein content was slightly lower in overexpressing AtATG8a and AtATG8g seedlings [31], suggesting that NBR1 degradation was stimulated in the ATG8 overexpression.…”

Full-length transcriptome sequencing of Arabidopsis plants provided new insights into the autophagic regulation of photosynthesis

“…Chloroplasts are the most important sites for photosynthesis. Two new studies have shown that autophagy is extensively involved in chloroplast degradation under abiotic stress, which may be one of the main reasons for the decline in plant photosynthetic capacity 59 , 60 .…”

Autophagy: a key player in the recovery of plants from heat stress

“…For years, autophagy has been recognized for its role in bulk and non-selective degradation of cytoplasmic constituents and organelles, particularly under conditions such as senescence or starvation. However, more studies have shed light on a new aspect of autophagy functionality: selective autophagy ( Derrien et al , 2012 ; Floyd et al , 2015 ; Thirumalaikumar et al , 2021 ; Tong et al , 2023 ; Wan et al , 2023 ). These studies have demonstrated that autophagy can operate selectively, targeting specific cellular components or macromolecules for degradation ( Fig.…”

“…Selective autophagy efficiently disposes of damaged or unneeded macromolecules (e.g. proteins and RNAs) or even organelles, as well as protein aggregates ( Derrien et al , 2012 ; Zhou et al , 2013 ; Floyd et al , 2015 ; Michaeli et al , 2016 , 2019 ; Tong et al , 2023 ; Wan et al , 2023 ). Autophagy is active in cells under normal growth conditions, operating at a basal level to maintain cellular homeostasis.…”

“…These studies indicate the essential role of autophagy in eliminating aggregated and toxic proteins following severe HS (basal thermotolerance) in plant cells. Furthermore, a more recent study demonstrated the involvement of NBR1 in mediating autophagic degradation of the TOC (Translocon at the Outer envelope membrane of Chloroplasts) complex in response to HS, thereby influencing chloroplast protein import and photosynthetic capacity ( Wan et al , 2023 ).…”