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Plants repress ROS1 expression to attenuate heat-induced transposon burst

Nature Plants volume 11, pages 1785–1797 (2025)Cite this article

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Abstract

The active DNA demethylase Repressor of Silencing 1 (ROS1) regulates genomic DNA methylation patterns during plant development. ROS1 expression is promoted by DNA methylation within its promoter region. However, the mechanisms and biological significance of ROS1 regulation under abiotic stresses remain elusive. Here we show that heat stress reduces DNA methylation in the ROS1 promoter to suppress its expression. Under normal conditions, SUVH1 and SUVH3 bind methylated ROS1 promoter regions, inhibiting chromatin interactions around the ROS1 locus; heat stress triggers their dissociation, enabling chromatin loop formation to suppress ROS1 transcription. Transgenic plants with exogenous ROS1 maintain high expression levels during heat stress, causing transposable element hypomethylation and enhanced transcription and transgenerational transposition of the heat-activated retrotransposon ONSEN. We propose that heat-induced suppression of ROS1 transcription, which is conserved across plant species, serves as a brake system to limit transposable element activation, thereby safeguarding genome stability.

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Fig. 1: Heat stress represses ROS1 expression by reducing DNA methylation within its promoter region.
Fig. 2: Heat stress represses ROS1 expression by enhancing local chromatin interactions around the enROS1 locus.
Fig. 3: ROS1 transgenic plants promote heat-induced ONSEN transcription and transposition.
Fig. 4: ROS1 regulates the expression of ONSEN through active DNA demethylation.
Fig. 5: Repressing ROS1 expression by heat stress is conserved across plant species.
Fig. 6: A working model of plants repressing ROS1 expression to attenuate heat-induced ONSEN transcription and transposition in Arabidopsis.

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Data availability

RNA-seq data of Col-0 under normal, heat stress and recovery conditions were previously deposited in Gene Expression Omnibus under accession number GSE132415. Hi-C data of Col-0 under normal and heat stress conditions were previously deposited in the National Center for Biotechnology Information Sequence Read Archive under accession number PRJNA545383. Methylome data (Col-0 under normal condition; Col-0, ros1-4 and SP:ROS1-GFP under heat stress) and ATAC-seq data (Col-0 under control versus heat stress) have been submitted to the China National Center for Bioinformation under accession number PRJCA036954 (the link for WGBS data is https://ngdc.cncb.ac.cn/gsa/s/UTraPW9M; the link for ATAC-seq data is https://ngdc.cncb.ac.cn/gsa/s/h6dC68Mx). All other supporting data are included in the article or its Supplementary Information. Source data are provided with this paper.

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Acknowledgements

We thank S. Jacobson for providing seeds of the suvh1 suvh3 mutant. This study was supported by the National Natural Science Foundation of China (32170285 to L.-M.F. and 32270288 to W.Q.) and Beijing Life Science Academy (BLSA: 2024500CA0010 to W.Q.).

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Author notes

  1. These authors contributed equally: Lingjiao Fan, Yuqing Jing.

Authors and Affiliations

  1. State Key Laboratory of Wheat Improvement, School of Advanced Agricultural Sciences, Peking University, Beijing, China

    Lingjiao Fan & Weiqiang Qian

  2. Beijing Life Science Academy, Beijing, China

    Lingjiao Fan & Weiqiang Qian

  3. State Key Laboratory for Gene Function and Modulation Research, School of Life Sciences, Peking University, Beijing, China

    Yuqing Jing, Xinyu Liu & Liu-Min Fan

  4. Academy for Advanced Interdisciplinary Studies, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China

    Wenxin Zhang

  5. Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agriculture Sciences in Weifang, Weifang, China

    Yingjie Mi

  6. College of Life Sciences, Nanjing Normal University, Nanjing, China

    Linhua Sun

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  1. Lingjiao Fan
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Contributions

L.F., L.-M.F. and W.Q. designed the research; L.F., Y.J. and X.L. performed the experiments and analysed the data; W.Z., Y.M. and L.S. performed the bioinformatics analysis. L.F. drafted the paper; L.-M.F. and W.Q. revised the paper.

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Correspondence to Weiqiang Qian.

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Nature Plants thanks Hidetaka Ito and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 ROS1 expression levels in the relative epigenetic mutants.

a, Quantification of ROS1 expression levels in Col-0, nrpd1-3, and nrpe1-11 under control and heat-stress conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed student’s t-test. b, Bisulfite sequencing data showing DNA methylation levels in the ROS1 MEMS region in rdd-2 under control and heat-stress conditions. At least 20 clones were sequenced for each sample. Each circle represents one biological replicate (n = 2 biological replicates). c, Quantification of ROS1 expression levels in Col-0, ros1-4, and rdd-2 under control and heat conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed student’s t-test.

Extended Data Fig. 2 Heat stress selectively targets the enROS1 locus rather than the exROS1 locus.

a, Quantification of total ROS1 transcript levels in Col-0 and NP:ROS1-LUC (ProROS1:ROS1-LUC/Col-0) transgenic lines. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed Student’s t-test. b, Quantification of total ROS1 transcript levels in Col-0 and NP:ROS1-Myc (ProROS1:ROS1-Myc/Col-0) transgenic lines. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed Student’s t-test. c, Quantification of enROS1 (left panel) and exROS1 (right panel) transcript levels in NP:ROS1-Myc transgenic lines under control and heat conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed Student’s t-test. d, Relative quantification of ROS1 transcript levels in Col-0 and SP:ROS1-GFP (super1300:ROS1-GFP/ros1-4) transgenic plants under control and heat-stress conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed Student’s t-test. e, Snapshots in the integrated Genome Browser (IGV) showing the ATAC-seq peak at the promoter of ROS1 (AT2G36490) in Col-0 under control (22 °C) and heat (37 °C) conditions.

Extended Data Fig. 3 SUVH1 binds DNA methylation in the ROS1 promoter and promotes ROS1 expression.

a, ChIP-qPCR assay analyzing the binding of SUVH1 at the ROS1 locus. The upper schematic illustrates the positions of primers (P1 - P3), and the lower column chart depicts the enrichment of SUVH1 at the ROS1 locus. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed Student’s t-test. b, Quantification of SUVH1 transcript levels in Col-0 and SUVH1-Flag transgenic plants under control and heat-stress conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-tailed Student’s t-test. c, Western blot analysis showing protein levels of SUVH1 under control (C) and heat-stress (H) conditions. ACTIN protein was used as the loading control. d, Quantification of ROS1 transcript levels in Col-0 and suvh1 suvh3 under control and heat-stress conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-way ANOVA with Bonferroni’s multiple comparisons test.

Source data

Extended Data Fig. 4 Overexpression of ROS1 under heat-stress conditions promotes TE expression.

Relative quantification of ROMANIAT5, AtMU1, and TSI transcript levels in Col-0 and ROS1 transgenic lines under control and heat conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-way ANOVA with Bonferroni’s multiple comparisons test.

Extended Data Fig. 5 ROS1 regulates TE expression via its demethylase activity.

a-c, IGV snapshots showing DNA methylation levels at ONSEN, ROMANIAT5, AtMU1, AtMU2 and AtGP10 loci in Col-0 (22 °C), Col-0 (37 °C), ros1-4 (37 °C) and SP:ROS1-GFP (37 °C) plants. TE promoter regions are highlighted by red boxes. d, Bisulfite sequencing data showing CHH methylation levels in the regions spanning upstream, LTR, and partial ORF of ONSEN2 (AT3TE92525) in Col-0 (22 °C), Col-0 (37 °C), and SP:ROS1-GFP (37 °C) plants. At least 20 clones were sequenced for each sample. Each circle represents one biological replicate (n = 2 biological replicates). LTR, long terminal repeat; ORF, open reading frame; Red line represents the genomic location of BS-PCR amplification products. e, Relative quantification of ROMANIAT5, AtMU1, and TSI expression levels in Col-0, SP:ROS1-Flag, and SP:ROS1C1045S-Flag transgenic lines under control and heat-stress conditions. Data represent mean ± s.d., n = 3 biological replicates. Two-way ANOVA with Bonferroni’s multiple comparisons test.

Supplementary information

Supplementary Information

Supplementary Figs. 1–4.

Reporting Summary

Supplementary Data 1

Primers and probes used in this study.

Supplementary Data 2

Information of ROS1 homologues in different species.

Supplementary Data 3

Statistical source data for Supplementary Fig. 2.

Source data

Source Data Extended Data Fig. 3

Uncropped western blots for Extended Dada Fig. 3c.

Source Data

Statistical source data.

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Fan, L., Jing, Y., Liu, X. et al. Plants repress ROS1 expression to attenuate heat-induced transposon burst. Nat. Plants 11, 1785–1797 (2025). https://doi.org/10.1038/s41477-025-02076-9

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