Hyperosmotic stress memory in Arabidopsis is mediated by a limited set of epigenetically labile DNA sequences and is restricted by DNA glycosylase activity in the male germline

Inducible epigenetic changes are believed to enable rapid adaptation to environmental fluctuations in eukaryotes. We have found a limited set of regions of the Arabidopsis genome that are specifically targeted for DNA (de)methylation in response to hyperosmotic stress. The stress-induced epigenetic changes are associated with conditionally heritable adaptive phenotypic stress responses, which are extensively reset in absence of stress. These stress responses are not transmitted equally from the two parents due to widespread DNA glycosylase activity in the male germline. Molecular analyses of the CNI1/ATL31 stress-response regulator further revealed that epigenetically targeted sequences function as distantly-acting control elements of antisense long non-coding RNAs that in turn regulate CNI1 expression in response to stress. Collectively, our findings reveal that plants have a highly dynamic ‘short-term stress memory’ with which to respond to adverse external conditions. This short-memory relies on discrete DNA methylation and associated transcriptional changes that extend the phenotypic space accessible to the immediate offspring.

人们普遍认为，可诱导的表观遗传（epigenetic）改变能够帮助真核生物快速适应环境波动。我们在拟南芥（Arabidopsis）基因组中发现了有限的若干区域，这些区域会在高渗胁迫下特异性地成为DNA（脱）甲基化的靶标。这类胁迫诱导的表观遗传改变，与条件可遗传的适应性表型胁迫响应相关，且在无胁迫条件下会被广泛重置。由于雄性生殖系中广泛存在的DNA糖苷酶（DNA glycosylase）活性，这类胁迫响应无法通过双亲均等传递给后代。对CNI1/ATL31胁迫响应调控因子的分子分析进一步揭示，表观遗传靶向序列可作为反义长链非编码RNA的远端作用调控元件，进而调控CNI1在胁迫响应中的表达。综上，我们的研究结果表明，植物拥有一套高度动态的‘短期胁迫记忆’，以此应对不利的外界环境。这类短期记忆依赖于特异性的DNA甲基化及相关转录改变，这些改变能够拓展当代后代可利用的表型空间。