Brassinosteroids act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato

The brassinosteroid signaling element BZR1 positively regulates autophagy-selective receptor NBR1 genes in tomato by directly binding to their promoters and promoting the degradation of ubiquitinated proteins, thus enhancing cold tolerance. Abstract Autophagy is a highly conserved and regulated cata...

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Veröffentlicht in:Journal of experimental botany 2020-01, Vol.71 (3), p.1092-1106
Hauptverfasser: Chi, Cheng, Li, Xiaomeng, Fang, Pingping, Xia, Xiaojian, Shi, Kai, Zhou, Yanhong, Zhou, Jie, Yu, Jingquan
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container_end_page 1106
container_issue 3
container_start_page 1092
container_title Journal of experimental botany
container_volume 71
creator Chi, Cheng
Li, Xiaomeng
Fang, Pingping
Xia, Xiaojian
Shi, Kai
Zhou, Yanhong
Zhou, Jie
Yu, Jingquan
description The brassinosteroid signaling element BZR1 positively regulates autophagy-selective receptor NBR1 genes in tomato by directly binding to their promoters and promoting the degradation of ubiquitinated proteins, thus enhancing cold tolerance. Abstract Autophagy is a highly conserved and regulated catabolic process involved in the degradation of protein aggregates, which plays critical roles in eukaryotes. In plants, multiple molecular processes can induce or suppress autophagy but the mechanism of its regulation by phytohormones is poorly understood. Brassinosteroids (BRs) are steroid phytohormones that play crucial roles in plant response to stresses. Here, we investigate the role of BRs in NBR1-dependent selective autophagy in response to chilling stress in tomato. BRs and their signaling element BZR1 can induce autophagy and accumulation of the selective autophagy receptor NBR1 in tomato under chilling stress. Cold increased the stability of BZR1, which was promoted by BRs. Cold- and BR-induced increased BZR1 stability activated the transcription of several autophagy-related genes (ATGs) and NBR1 genes by directly binding to their promoters, which resulted in selective autophagy. Furthermore, silencing of these ATGs or NBR1 genes resulted in a decreased accumulation of several functional proteins and an increased accumulation of ubiquitinated proteins, subsequently compromising BR-induced cold tolerance. These results strongly suggest that BRs regulate NBR1-dependent selective autophagy in a BZR1-dependent manner in response to chilling stress in tomato.
doi_str_mv 10.1093/jxb/erz466
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Abstract Autophagy is a highly conserved and regulated catabolic process involved in the degradation of protein aggregates, which plays critical roles in eukaryotes. In plants, multiple molecular processes can induce or suppress autophagy but the mechanism of its regulation by phytohormones is poorly understood. Brassinosteroids (BRs) are steroid phytohormones that play crucial roles in plant response to stresses. Here, we investigate the role of BRs in NBR1-dependent selective autophagy in response to chilling stress in tomato. BRs and their signaling element BZR1 can induce autophagy and accumulation of the selective autophagy receptor NBR1 in tomato under chilling stress. Cold increased the stability of BZR1, which was promoted by BRs. Cold- and BR-induced increased BZR1 stability activated the transcription of several autophagy-related genes (ATGs) and NBR1 genes by directly binding to their promoters, which resulted in selective autophagy. Furthermore, silencing of these ATGs or NBR1 genes resulted in a decreased accumulation of several functional proteins and an increased accumulation of ubiquitinated proteins, subsequently compromising BR-induced cold tolerance. These results strongly suggest that BRs regulate NBR1-dependent selective autophagy in a BZR1-dependent manner in response to chilling stress in tomato.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erz466</identifier><identifier>PMID: 31639824</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Autophagy ; Beclin-1 - metabolism ; Brassinosteroids - metabolism ; Cold-Shock Response ; Lycopersicon esculentum - physiology ; Proteostasis</subject><ispartof>Journal of experimental botany, 2020-01, Vol.71 (3), p.1092-1106</ispartof><rights>The Author(s) 2019. 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Abstract Autophagy is a highly conserved and regulated catabolic process involved in the degradation of protein aggregates, which plays critical roles in eukaryotes. In plants, multiple molecular processes can induce or suppress autophagy but the mechanism of its regulation by phytohormones is poorly understood. Brassinosteroids (BRs) are steroid phytohormones that play crucial roles in plant response to stresses. Here, we investigate the role of BRs in NBR1-dependent selective autophagy in response to chilling stress in tomato. BRs and their signaling element BZR1 can induce autophagy and accumulation of the selective autophagy receptor NBR1 in tomato under chilling stress. Cold increased the stability of BZR1, which was promoted by BRs. Cold- and BR-induced increased BZR1 stability activated the transcription of several autophagy-related genes (ATGs) and NBR1 genes by directly binding to their promoters, which resulted in selective autophagy. 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subjects Autophagy
Beclin-1 - metabolism
Brassinosteroids - metabolism
Cold-Shock Response
Lycopersicon esculentum - physiology
Proteostasis
title Brassinosteroids act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato
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