Cooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in Arabidopsis

Abstract Dissecting the mechanisms underlying heat tolerance is important for understanding how plants acclimate to heat stress. Here, we identify a heat-responsive gene in Arabidopsis thaliana, RNA-DIRECTED DNA METHYLATION 16 (RDM16), which encodes a pre-mRNA splicing factor. Knockout mutants of RD...

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Main Authors: Jing Ma, Shuai Li, Tengyue Wang, Zhen Tao, Shijie Huang, Ning Lin, Yibing Zhao, Chuanhong Wang, Peijin Li
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-55850-w
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author Jing Ma
Shuai Li
Tengyue Wang
Zhen Tao
Shijie Huang
Ning Lin
Yibing Zhao
Chuanhong Wang
Peijin Li
author_facet Jing Ma
Shuai Li
Tengyue Wang
Zhen Tao
Shijie Huang
Ning Lin
Yibing Zhao
Chuanhong Wang
Peijin Li
author_sort Jing Ma
collection DOAJ
description Abstract Dissecting the mechanisms underlying heat tolerance is important for understanding how plants acclimate to heat stress. Here, we identify a heat-responsive gene in Arabidopsis thaliana, RNA-DIRECTED DNA METHYLATION 16 (RDM16), which encodes a pre-mRNA splicing factor. Knockout mutants of RDM16 are hypersensitive to heat stress, which is associated with impaired splicing of the mRNAs of 18 out of 20 HEAT SHOCK TRANSCRIPTION FACTOR (HSF) genes. RDM16 forms condensates upon exposure to heat. The arginine residues in intrinsically disordered region 1 (IDR1) of RDM16 are responsible for RDM16 condensation and its function in heat stress tolerance. Notably, RDM16 produces two alternatively spliced transcripts designated RDM16-LONG (RDL) and RDM16-SHORT (RDS). RDS also forms condensates and can promote RDL condensation to improve heat tolerance. Our findings provide insight into the cooperative condensation of the two RDM16 isoforms encoded by RDM16 splice variants in enhancing heat tolerance in Arabidopsis.
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institution Kabale University
issn 2041-1723
language English
publishDate 2025-01-01
publisher Nature Portfolio
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series Nature Communications
spelling doaj-art-b9c0483d9b394a49bfc645746007f0f32025-01-12T12:30:01ZengNature PortfolioNature Communications2041-17232025-01-0116111610.1038/s41467-025-55850-wCooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in ArabidopsisJing Ma0Shuai Li1Tengyue Wang2Zhen Tao3Shijie Huang4Ning Lin5Yibing Zhao6Chuanhong Wang7Peijin Li8The National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityThe National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural UniversityAbstract Dissecting the mechanisms underlying heat tolerance is important for understanding how plants acclimate to heat stress. Here, we identify a heat-responsive gene in Arabidopsis thaliana, RNA-DIRECTED DNA METHYLATION 16 (RDM16), which encodes a pre-mRNA splicing factor. Knockout mutants of RDM16 are hypersensitive to heat stress, which is associated with impaired splicing of the mRNAs of 18 out of 20 HEAT SHOCK TRANSCRIPTION FACTOR (HSF) genes. RDM16 forms condensates upon exposure to heat. The arginine residues in intrinsically disordered region 1 (IDR1) of RDM16 are responsible for RDM16 condensation and its function in heat stress tolerance. Notably, RDM16 produces two alternatively spliced transcripts designated RDM16-LONG (RDL) and RDM16-SHORT (RDS). RDS also forms condensates and can promote RDL condensation to improve heat tolerance. Our findings provide insight into the cooperative condensation of the two RDM16 isoforms encoded by RDM16 splice variants in enhancing heat tolerance in Arabidopsis.https://doi.org/10.1038/s41467-025-55850-w
spellingShingle Jing Ma
Shuai Li
Tengyue Wang
Zhen Tao
Shijie Huang
Ning Lin
Yibing Zhao
Chuanhong Wang
Peijin Li
Cooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in Arabidopsis
Nature Communications
title Cooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in Arabidopsis
title_full Cooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in Arabidopsis
title_fullStr Cooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in Arabidopsis
title_full_unstemmed Cooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in Arabidopsis
title_short Cooperative condensation of RNA-DIRECTED DNA METHYLATION 16 splicing isoforms enhances heat tolerance in Arabidopsis
title_sort cooperative condensation of rna directed dna methylation 16 splicing isoforms enhances heat tolerance in arabidopsis
url https://doi.org/10.1038/s41467-025-55850-w
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