Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.
Department of Plant Physiology, Aachen Biology and Biotechnology, RWTH Aachen University, Aachen, Germany.
Mol Plant Pathol. 2021 Jan;22(1):19-30. doi: 10.1111/mpp.13005. Epub 2020 Oct 19.
Systemic acquired resistance (SAR) is a broad-spectrum disease resistance response that can be induced upon infection from pathogens or by chemical treatment, such as with benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH). SAR involves priming for more robust activation of defence genes upon pathogen attack. Whether priming for SAR would involve components of RNA silencing remained unknown. Here, we show that upon leaf infiltration of water, BTH-primed Arabidopsis thaliana plants accumulate higher amounts of mRNA of ARGONAUTE (AGO)2 and AGO3, key components of RNA silencing. The enhanced AGO2 expression is associated with prior-to-activation trimethylation of lysine 4 in histone H3 and acetylation of histone H3 in the AGO2 promoter and with induced resistance to the yellow strain of cucumber mosaic virus (CMV[Y]). The results suggest that priming A. thaliana for enhanced defence involves modification of histones in the AGO2 promoter that condition AGO2 for enhanced activation, associated with resistance to CMV(Y). Consistently, the fold-reduction in CMV(Y) coat protein accumulation by BTH pretreatment was lower in ago2 than in wild type, pointing to reduced capacity of ago2 to activate BTH-induced CMV(Y) resistance. A role of AGO2 in pathogen-induced SAR is suggested by the enhanced activation of AGO2 after infiltrating systemic leaves of plants expressing a localized hypersensitive response upon CMV(Y) infection. In addition, local inoculation of SAR-inducing Pseudomonas syringae pv. maculicola causes systemic priming for enhanced AGO2 expression. Together our results indicate that defence priming targets the AGO2 component of RNA silencing whose enhanced expression is likely to contribute to SAR.
系统获得性抗性 (SAR) 是一种广谱的抗病性反应，可以在病原体感染或化学处理（如苯并-[1,2,3]-噻二唑-7-羧酸 S-甲酯 (BTH)）后诱导。SAR 涉及在病原体攻击时为防御基因的更强烈激活做好准备。SAR 的启动是否会涉及 RNA 沉默的成分尚不清楚。在这里，我们表明，在叶片浸润水后，BTH 诱导的拟南芥植物积累了更多的 ARGONAUTE (AGO)2 和 AGO3 的 mRNA，这是 RNA 沉默的关键成分。增强的 AGO2 表达与组蛋白 H3 赖氨酸 4 的激活前三甲基化和 AGO2 启动子中的组蛋白 H3 乙酰化有关，并与对黄瓜花叶病毒 (CMV[Y]) 的黄株的抗性有关。结果表明，为增强防御而启动拟南芥涉及AGO2 启动子中组蛋白的修饰，该修饰使 AGO2 能够增强激活，与对 CMV(Y) 的抗性有关。一致地，BTH 预处理降低了 CMV(Y)外壳蛋白积累的倍数，在 ago2 中比在野生型中降低，表明 ago2 激活 BTH 诱导的 CMV(Y) 抗性的能力降低。通过感染表达局部过敏反应的植物的系统性叶片后，AGO2 的增强激活表明 AGO2 在病原体诱导的 SAR 中发挥作用。此外，SAR 诱导的丁香假单胞菌 pv。maculicola 的局部接种会导致增强的 AGO2 表达的系统性启动。总之，我们的结果表明，防御启动针对 RNA 沉默的 AGO2 成分，其增强的表达可能有助于 SAR。
