Sequestration of DBR1 to stress granules promotes lariat intronic RNAs accumulation for heat-stress tolerance

Chengyun Wu, Xingsong Wang, Yan Li, Weibo Zhen, Chunfei Wang, Xiaoqing Wang, Zhouli Xie, Xiumei Xu, Siyi Guo, José Ramón Botella, Binglian Zheng, Wei Wang, Chun-Peng Song () and Zhubing Hu ()
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Chengyun Wu: Henan University
Xingsong Wang: Henan University
Yan Li: Henan University
Weibo Zhen: Henan University
Chunfei Wang: Henan University
Xiaoqing Wang: Henan University
Zhouli Xie: Peking University
Xiumei Xu: Henan University
Siyi Guo: Henan University
José Ramón Botella: The University of Queensland
Binglian Zheng: Fudan University
Wei Wang: Peking University
Chun-Peng Song: Henan University
Zhubing Hu: Henan University

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Heat stress (HS) poses a significant challenge to plant survival, necessitating sophisticated molecular mechanisms to maintain cellular homeostasis. Here, we identify SICKLE (SIC) as a key modulator of HS responses in Arabidopsis (Arabidopsis thaliana). SIC is required for the sequestration of RNA DEBRANCHING ENZYME 1 (DBR1), a rate-limiting enzyme of lariat intronic RNA (lariRNA) decay, into stress granules (SGs). The sequestration of DBR1 by SIC enhances the accumulation of lariRNAs, branched circular RNAs derived from excised introns during pre-mRNA splicing, which in turn promote the transcription of their parental genes. Our findings further demonstrate that SIC-mediated DBR1 sequestration in SGs is crucial for plant HS tolerance, as deletion of the N-terminus of SIC (SIC1–244) impairs DBR1 sequestration and compromises plant response to HS. Overall, our study unveils a mechanism of transcriptional regulation in the HS response, where lariRNAs are enriched through DBR1 sequestration, ultimately promoting the transcription of heat stress tolerance genes.

Date: 2024
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DOI: 10.1038/s41467-024-52034-w

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