Sequestration of DBR1 to stress granules promotes lariat intronic RNAs accumulation for heat-stress tolerance
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 (SIC<sup>1-244</sup>) 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.
Authors
- José Ramón Botella (ORCID: https://orcid.org/0000-0002-4446-3432)
- Binglian Zheng (ORCID: https://orcid.org/0000-0001-5650-5348)
- Zhubing Hu (ORCID: https://orcid.org/0000-0002-5394-9864)
- X. Wang (ORCID: https://orcid.org/0009-0005-8466-4852)
- Weibo Zhen (ORCID: https://orcid.org/0000-0002-4120-331X)
- Siyi Guo (ORCID: https://orcid.org/0000-0003-2013-1772)
- Zhouli Xie (ORCID: https://orcid.org/0000-0001-6494-4949)
- Chengyun Wu (ORCID: https://orcid.org/0000-0002-8202-5134)
- Xiaoqing Wang (ORCID: https://orcid.org/0000-0001-7476-8889)
- Wei Wang (ORCID: https://orcid.org/0000-0002-3780-5158)
- Yan Li (ORCID: https://orcid.org/0000-0001-7425-2524)
- Xiumei Xu
- Chun‐Peng Song (ORCID: https://orcid.org/0000-0001-8774-4309)
- Chunfei Wang (ORCID: https://orcid.org/0000-0003-1738-2490)
Institutions
- Anhui Agricultural University (CN)
- The University of Queensland (AU)
- Henan University (CN)
- Peking University (CN)
- Fudan University (CN)
- Sanya University (CN)
- ARC Centre of Excellence for Plant Success in Nature and Agriculture (AU)
- Center for Life Sciences (CN)
- State Key Laboratory of Genetic Engineering
Publication Details
- Journal
- Nature Communications
- Published
- 2024-09-03
- DOI
- https://doi.org/10.1038/s41467-024-52034-w
- Citations
- 13
- Primary Topic
- RNA Research and Splicing
- Type
- article
- Field-Weighted Citation Impact
- 3.04