Chavan Satish Namdeo, Degroote Eva, De Kock Karen, Demeestere Kristof, Kyndt Tina
Faculty of Bioscience Engineering, Department of Biotechnology, Ghent University, Proeftuinstraat 86 N1, Ghent 9000, Belgium.
ICAR-Indian Institute of Rice Research, Department of Nematology, Rajendranagar, Hyderabad 500030, India.
Plant Physiol. 2024 Dec 23;197(1). doi: 10.1093/plphys/kiae598.
Plants can transmit information to the next generation and modulate the phenotype of their offspring through epigenetic mechanisms. In this study, we demonstrate the activation of "intergenerational acquired resistance" (IAR) in the progeny of rice (Oryza sativa) plants exogenously treated with dehydroascorbate (DHA). The offspring of lifelong DHA-treated plants (DHA-IAR) were significantly less susceptible to the root-knot nematode Meloidogyne graminicola and partially inherited the DHA-induced transcriptional response found in the parental plants. Phytohormone analyses on the DHA-IAR plants unveiled higher basal abscisic acid levels and a primed induction of the jasmonic acid pathway. RNA-seq analysis on the embryonic tissues of immature seeds of DHA-treated plants revealed major shifts in the expression of genes associated with epigenetic pathways. We confirmed that DHA treatment leads to a significant but transient pattern of global DNA hypomethylation in the parental plants 12 to 24 h after treatment. The induction of resistance in the parental plants requires the DNA demethylase REPRESSOR OF SILENCING 1C (ROS1c) and ARGONAUTE 4, suggesting a role for DNA demethylation and subsequent remethylation in establishment of this phenotype. Confirming the transience of global hypomethylation upon DHA treatment, no significant change in global DNA methylation levels was observed in DHA-IAR versus naïve plants. Finally, DHA could not induce IAR in the ros1c mutant line and the ARGONAUTE 4 (ago4ab)-RNAi line. These data indicate that a controlled collaboration between transient DNA demethylation and remethylation underlies the induced resistance and IAR phenotypes upon DHA treatment.
植物能够通过表观遗传机制向下一代传递信息并调节其后代的表型。在本研究中，我们证明了用脱氢抗坏血酸（DHA）外源处理的水稻（Oryza sativa）植株的后代中“代际获得性抗性”（IAR）被激活。经终生DHA处理的植株（DHA-IAR）的后代对根结线虫Meloidogyne graminicola的易感性显著降低，并部分继承了亲本植株中DHA诱导的转录反应。对DHA-IAR植株的植物激素分析表明，其基础脱落酸水平较高，茉莉酸途径被引发诱导。对DHA处理植株未成熟种子的胚组织进行RNA测序分析，揭示了与表观遗传途径相关基因表达的主要变化。我们证实，DHA处理导致亲本植株在处理后12至24小时出现显著但短暂的全基因组DNA低甲基化模式。亲本植株中抗性的诱导需要DNA去甲基化酶沉默抑制因子1C（ROS1c）和AGO4，这表明DNA去甲基化及随后的重新甲基化在该表型的建立中起作用。证实了DHA处理后全基因组低甲基化的短暂性，在DHA-IAR植株与未经处理的植株相比，未观察到全基因组DNA甲基化水平有显著变化。最后，DHA不能在ros1c突变系和AGO4（ago4ab）-RNAi系中诱导IAR。这些数据表明，短暂的DNA去甲基化和重新甲基化之间的协同作用是DHA处理后诱导抗性和IAR表型的基础。
