Inheritance of acquired adaptive cold tolerance in rice through DNA methylation
Epigenetic pathways could provide a mechanistic explanation for the inheritance of acquired characteristics, as proposed by Lamarck in 1802, but epigenetic alterations that endow adaptive hereditary traits have rarely been observed. Here, in cultivated Asian rice (Oryzasativa L.), we identified an epiallele conferring acquired and heritable cold tolerance, an adaptive trait enabling northward spread from its tropical origins. We subjected cold-sensitive rice to multigenerational cold stress and identified a line with acquired stable inheritance of cold tolerance. DNA-hypomethylation variation in the acquiredcoldtolerance 1 (ACT1) promoter region rendered its expression insensitive to cold. This change is, in large part, responsible for the acquired cold tolerance, as confirmed by DNA-methylation editing. Natural variation in ACT1 DNA hypomethylation is associated with cold tolerance and rice geographic distribution. Hypomethylation at ACT1 triggers adaptive cold tolerance, presenting a route to epigenetic-variation-driven inheritance of acquired characteristics.
Authors
- Baoshan Wang (ORCID: https://orcid.org/0000-0001-7203-9703)
- Jiang Shu (ORCID: https://orcid.org/0000-0003-3671-4665)
- Xianwei Song (ORCID: https://orcid.org/0009-0003-6331-4189)
- Shanjie Tang (ORCID: https://orcid.org/0000-0002-1634-6503)
- Xiaofeng Cao (ORCID: https://orcid.org/0000-0001-9871-0753)
- Lizhi Wang (ORCID: https://orcid.org/0000-0003-3074-4273)
- Xiuli Hou (ORCID: https://orcid.org/0000-0002-9373-3689)
- Zhenhua Guo
- Xian Deng (ORCID: https://orcid.org/0000-0003-2606-1525)
- Chao Yang (ORCID: https://orcid.org/0000-0001-8927-9391)
- Ying Meng (ORCID: https://orcid.org/0009-0004-3793-1850)
- Hui Liu (ORCID: https://orcid.org/0000-0002-1031-5669)
- Bin Yan
- H. Luo (ORCID: https://orcid.org/0009-0009-7187-1958)
Institutions
- Kunming Institute of Botany (CN)
- Northwestern Polytechnical University (CN)
- Chinese Academy of Sciences (CN)
- Institute of Genetics and Developmental Biology (CN)
- University of Chinese Academy of Sciences (CN)
Publication Details
- Journal
- Cell
- Published
- 2025-05-22
- DOI
- https://doi.org/10.1016/j.cell.2025.04.036
- Citations
- 53
- Primary Topic
- Plant Molecular Biology Research
- Type
- article
- Field-Weighted Citation Impact
- 92.74
Funders
- Northwestern University
- National Natural Science Foundation of China
- Chinese Academy of Sciences
- Northwestern Polytechnical University
- China Postdoctoral Science Foundation
- National Key Research and Development Program of China
- Institute of Botany, Chinese Academy of Sciences
- Youth Innovation Promotion Association
- Institute of Genetics and Developmental Biology, Chinese Academy of Sciences
- Institute of Genetics