Inheritance of acquired adaptive cold tolerance in rice through DNA methylation
Xianwei Song, Shanjie Tang, Hui Liu, Ying Meng, Haofei Luo, Baoshan Wang, Xiuli Hou, Bin Yan, Chao Yang, Zhenhua Guo, Lizhi Wang, Jiang Shu, Xian Deng, Xiaofeng Cao
Abstract
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.