A converged ubiquitin-proteasome pathway for the degradation of TOC and TOM tail-anchored receptors

doi:10.1111/jipb.13645

J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (5): 1007-1023.DOI: 10.1111/jipb.13645

• Research Articles • Previous Articles Next Articles

A converged ubiquitin-proteasome pathway for the degradation of TOC and TOM tail-anchored receptors

Meijing Yang^{1, 2†}, Shuai Chen^{3, 4†}, Shey-Li Lim¹, Lang Yang^{1, 2}, Jia Yi Zhong¹, Koon Chuen Chan¹, Zhizhu Zhao¹, Kam-Bo Wong^{4, 5}, Junqi Wang² and Boon Leong Lim^{1, 5, 6*}

1. School of Biological Sciences, University of Hong Kong, Pokfulam 999077, Hong Kong, China
2. Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China
3. School of Biomedical Engineering, Shenzhen University, Shenzhen 518060, China
4. School of Life Sciences, The Chinese University of Hong Kong, Shatin 999077, Hong Kong, China
5. State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin 999077, Hong Kong, China
6. HKU Shenzhen Institute of Research and Innovation, Shenzhen 518052, China
^†These authors contributed equally to this work.
^*Correspondence:Boon Leong Lim (bllim@hku.hk)

Received:2023-12-06 Accepted:2024-02-27 Online:2024-03-19 Published:2024-05-01

Abstract

Abstract: In plants, thousands of nucleus-encoded proteins translated in the cytosol are sorted to chloroplasts and mitochondria by binding to specific receptors of the TOC (translocon on the outer chloroplast membrane) and the TOM (translocon on the outer mitochondrial membrane) complexes for import into those organelles. The degradation pathways for these receptors are unclear. Here, we discovered a converged ubiquitin-proteasome pathway for the degradation of Arabidopsis thaliana TOC and TOM tail-anchored receptors. The receptors are ubiquitinated by E3 ligase(s) and pulled from the outer membranes by the AAA⁺ adenosine triphosphatase CDC48, after which a previously uncharacterized cytosolic protein, transmembrane domain (TMD)-binding protein for tail-anchored outer membrane proteins (TTOP), binds to the exposed TMDs at the C termini of the receptors and CDC48, and delivers these complexes to the 26S proteasome.

Key words: 26S proteasome, CDC48, SP1, TOC, TOM, ubiquitination

Meijing Yang, Shuai Chen, Shey-Li Lim, Lang Yang, Jia Yi Zhong, Koon Chuen Chan, Zhizhu Zhao, Kam-Bo Wong, Junqi Wang and Boon Leong Lim. A converged ubiquitin-proteasome pathway for the degradation of TOC and TOM tail-anchored receptors[J]. J Integr Plant Biol., 2024, 66(5): 1007-1023.

[1]	Gao-Ping Qu, Bochen Jiang and Chentao Lin. The dual-action mechanism of Arabidopsis cryptochromes [J]. J Integr Plant Biol., 2024, 66(5): 883-896.
[2]	Young-Joon Park, Bo Eun Nam and Chung-Mo Park. Environmentally adaptive reshaping of plant photomorphogenesis by karrikin and strigolactone signaling [J]. J Integr Plant Biol., 2024, 66(5): 865-882.
[3]	Jun Yang, Ridong Chen, Chao Wang, Chun Li, Weizhen Ye, Zhonghui Zhang and Shouchuang Wang. A widely targeted metabolite modificomics strategy for modified metabolites identification in tomato [J]. J Integr Plant Biol., 2024, 66(4): 810-823.
[4]	Xiufen Dong, Xianfeng Liu, Lina Cheng, Ruizhen Li, Siqi Ge, Sai Wang, Yue Cai, Yang Liu, Sida Meng, Cai-Zhong Jiang, Chun-Lin Shi, Tianlai Li, Daqi Fu, Mingfang Qi and Tao Xu. SlBEL11 regulates flavonoid biosynthesis, thus fine-tuning auxin efflux to prevent premature fruit drop in tomato [J]. J Integr Plant Biol., 2024, 66(4): 749-770.
[5]	Citao Liu, Bigang Mao, Yanxia Zhang, Lei tian, Biao Ma, Zhuo Chen, Zhongwei Wei, Aifu Li, Ye Shao, Gongye Cheng, Lingling Li, Wenyu Li, Di Zhang, Xiaoping Ding, Jiangxiang Peng, Yulin Peng, Jiwai He, Nenghui Ye, Dingyang Yuan, Chengcai Chu and Meijuan Duan. The OsWRKY72-OsAAT30/OsGSTU26 module mediates reactive oxygen species scavenging to drive heterosis for salt tolerance in hybrid rice [J]. J Integr Plant Biol., 2024, 66(4): 709-730.
[6]	Jingbo Zhang, Xuexue Chen, Yajing Song and Zhizhong Gong. Integrative regulatory mechanisms of stomatal movements under changing climate [J]. J Integr Plant Biol., 2024, 66(3): 368-393.
[7]	Hayeon Kim, Hye Won Kang, Dae Yeon Hwang, Nayoung Lee, Akane Kubota, Takato Imaizumi and Young Hun Song. Low temperature-mediated repression and far-red light-mediated induction determine morning FLOWERING LOCUS T expression levels [J]. J Integr Plant Biol., 2024, 66(1): 103-120.
[8]	Danqi Zeng, Can Si, Mingze Zhang, Jun Duan and Chunmei He. ERF5 enhances protocorm-like body regeneration via enhancement of STM expression in Dendrobium orchid [J]. J Integr Plant Biol., 2023, 65(9): 2071-2085.
[9]	Jian‐Ping An, Hong‐Liang Li, Zhi‐Ying Liu, Da‐Ru Wang, Chun‐Xiang You and Yuepeng Han. The E3 ubiquitin ligase SINA1 and the protein kinase BIN2 cooperatively regulate PHR1 in apple anthocyanin biosynthesis [J]. J Integr Plant Biol., 2023, 65(9): 2175-2193.
[10]	Nini Ma, Nian Li, Zhongmao Yu, Chunli Chen, Dao‐Xiu Zhou and Yu Zhao. The F-box protein SHORT PRIMARY ROOT modulates primary root meristem activity by targeting SEUSS-LIKE protein for degradation in rice [J]. J Integr Plant Biol., 2023, 65(8): 1937-1949.
[11]	Fanliang Meng, Haoran Liu, Songshen Hu, Chengguo Jia, Min Zhang, Songwen Li, Yuanyuan Li, Jiayao Lin, Yue Jian, Mengyu Wang, Zhiyong Shao, Yuanyu Mao, Lihong Liu and Qiaomei Wang. The brassinosteroid signaling component SlBZR1 promotes tomato fruit ripening and carotenoid accumulation [J]. J Integr Plant Biol., 2023, 65(7): 1794-1813.
[12]	Irene Julca, Daniela Mutwil-Anderwald, Vaishnervi Manoj, Zahra Khan, Soak Kuan Lai, Lay K. Yang, Ing T. Beh, Jerzy Dziekan, Yoon P. Lim, Shen K. Lim, Yee W. Low, Yuen I. Lam, Seth Tjia, Yuguang Mu, Qiao W. Tan, Przemyslaw Nuc, Le M. Choo, Gillian Khew, Loo Shining, Antony Kam, James P. Tam, Zbynek Bozdech, Maximilian Schmidt, Bjoern Usadel, Yoganathan Kanagasundaram, Saleh Alseekh, Alisdair Fernie, Hoi Y. Li and Marek Mutwil. Genomic, transcriptomic, and metabolomic analysis of Oldenlandia corymbosa reveals the biosynthesis and mode of action of anti-cancer metabolites [J]. J Integr Plant Biol., 2023, 65(6): 1442-1466.
[13]	Junho Lee, Byeongho Moon, Dong Wook Lee and Inhwan Hwang. Translation rate underpins specific targeting of N-terminal transmembrane proteins to mitochondria [J]. J Integr Plant Biol., 2023, 65(6): 1505-1520.
[14]	Yingqi Hong, Yanxi Lv, Jianyi Zhang, Naveed Ahmad, Xiaokun Li, Na Yao, Xiuming Liu and Haiyan Li. The safflower MBW complex regulates HYSA accumulation through degradation by the E3 ligase CtBB1 [J]. J Integr Plant Biol., 2023, 65(5): 1277-1296.
[15]	Guojin Zhang, Yi Hu, Ming‐Zhong Huang, Wei‐Chang Huang, Ding‐Kun Liu, Diyang Zhang, Haihua Hu, Jason L. Downing, Zhong‐Jian Liu and Hong Ma. Comprehensive phylogenetic analyses of Orchidaceae using nuclear genes and evolutionary insights into epiphytism [J]. J Integr Plant Biol., 2023, 65(5): 1204-1225.

A converged ubiquitin-proteasome pathway for the degradation of TOC and TOM tail-anchored receptors

HTML

PDF

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments