Stress granules sequester autophagy proteins to facilitate plant recovery from heat stress
Abstract The autophagy pathway regulates the degradation of misfolded proteins caused by heat stress (HS) in the cytoplasm, thereby maintaining cellular homeostasis. Although previous studies have established that autophagy (ATG) genes are transcriptionally upregulated in response to HS, the precise...
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| Format: | Article |
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Nature Portfolio
2024-12-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55292-w |
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| author | Xibao Li Jun Liao Ka Kit Chung Lei Feng Yanglan Liao Zhixin Yang Chuanliang Liu Jun Zhou Wenjin Shen Hongbo Li Chengwei Yang Xiaohong Zhuang Caiji Gao |
| author_facet | Xibao Li Jun Liao Ka Kit Chung Lei Feng Yanglan Liao Zhixin Yang Chuanliang Liu Jun Zhou Wenjin Shen Hongbo Li Chengwei Yang Xiaohong Zhuang Caiji Gao |
| author_sort | Xibao Li |
| collection | DOAJ |
| description | Abstract The autophagy pathway regulates the degradation of misfolded proteins caused by heat stress (HS) in the cytoplasm, thereby maintaining cellular homeostasis. Although previous studies have established that autophagy (ATG) genes are transcriptionally upregulated in response to HS, the precise regulation of ATG proteins at the subcellular level remains poorly understood. In this study, we provide compelling evidence for the translocation of key autophagy components, including the ATG1/ATG13 kinase complex (ATG1a, ATG13a), PI3K complex (ATG6, VPS34), and ATG8-PE system (ATG5), to HS-induced stress granules (SGs) in Arabidopsis thaliana. As HS subsides, SGs disassemble, leading to the re-translocation of ATG proteins back to the cytoplasm, thereby facilitating the rapid activation of autophagy to degrade HS-induced ubiquitinated aggregates. Notably, autophagy activation is delayed in the SG-deficient (ubp1abc) mutants during the HS recovery phase, resulting in an insufficient clearance of ubiquitinated insoluble proteins that arise due to HS. Collectively, this study uncovers a previously unknown function of SGs in regulating autophagy as a temporary repository for ATG proteins under HS and provides valuable insights into the cellular mechanisms that maintain protein homeostasis during stress. |
| format | Article |
| id | doaj-art-7d7f13696e8e49ada553b4e4cc9cb8f8 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-7d7f13696e8e49ada553b4e4cc9cb8f82025-01-05T12:36:12ZengNature PortfolioNature Communications2041-17232024-12-0115111610.1038/s41467-024-55292-wStress granules sequester autophagy proteins to facilitate plant recovery from heat stressXibao Li0Jun Liao1Ka Kit Chung2Lei Feng3Yanglan Liao4Zhixin Yang5Chuanliang Liu6Jun Zhou7Wenjin Shen8Hongbo Li9Chengwei Yang10Xiaohong Zhuang11Caiji Gao12Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityCentre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong KongGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityCentre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong KongGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityAbstract The autophagy pathway regulates the degradation of misfolded proteins caused by heat stress (HS) in the cytoplasm, thereby maintaining cellular homeostasis. Although previous studies have established that autophagy (ATG) genes are transcriptionally upregulated in response to HS, the precise regulation of ATG proteins at the subcellular level remains poorly understood. In this study, we provide compelling evidence for the translocation of key autophagy components, including the ATG1/ATG13 kinase complex (ATG1a, ATG13a), PI3K complex (ATG6, VPS34), and ATG8-PE system (ATG5), to HS-induced stress granules (SGs) in Arabidopsis thaliana. As HS subsides, SGs disassemble, leading to the re-translocation of ATG proteins back to the cytoplasm, thereby facilitating the rapid activation of autophagy to degrade HS-induced ubiquitinated aggregates. Notably, autophagy activation is delayed in the SG-deficient (ubp1abc) mutants during the HS recovery phase, resulting in an insufficient clearance of ubiquitinated insoluble proteins that arise due to HS. Collectively, this study uncovers a previously unknown function of SGs in regulating autophagy as a temporary repository for ATG proteins under HS and provides valuable insights into the cellular mechanisms that maintain protein homeostasis during stress.https://doi.org/10.1038/s41467-024-55292-w |
| spellingShingle | Xibao Li Jun Liao Ka Kit Chung Lei Feng Yanglan Liao Zhixin Yang Chuanliang Liu Jun Zhou Wenjin Shen Hongbo Li Chengwei Yang Xiaohong Zhuang Caiji Gao Stress granules sequester autophagy proteins to facilitate plant recovery from heat stress Nature Communications |
| title | Stress granules sequester autophagy proteins to facilitate plant recovery from heat stress |
| title_full | Stress granules sequester autophagy proteins to facilitate plant recovery from heat stress |
| title_fullStr | Stress granules sequester autophagy proteins to facilitate plant recovery from heat stress |
| title_full_unstemmed | Stress granules sequester autophagy proteins to facilitate plant recovery from heat stress |
| title_short | Stress granules sequester autophagy proteins to facilitate plant recovery from heat stress |
| title_sort | stress granules sequester autophagy proteins to facilitate plant recovery from heat stress |
| url | https://doi.org/10.1038/s41467-024-55292-w |
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