Primary infection of a plant with a pathogen that causes high accumulation of salicylic acid in the plant typically via a hypersensitive response confers enhanced resistance against secondary infection with a broad spectrum of pathogens, including viruses. This phenomenon is called systemic acquired resistance (SAR), which is a plant priming for adaption to repeated biotic stress. However, the molecular mechanisms of SAR-mediated enhanced inhibition, especially of virus infection, remain unclear. Here, we show that SAR against cucumber mosaic virus (CMV) in tobacco plants (Nicotiana tabacum) involves a calmodulin-like protein, rgs-CaM. We previously reported the antiviral function of rgs-CaM, which binds to and directs degradation of viral RNA silencing suppressors (RSSs), including CMV 2b, via autophagy. We found that rgs-CaM-mediated immunity is ineffective against CMV infection in normally growing tobacco plants but is activated as a result of SAR induction via salicylic acid signaling. We then analyzed the effect of overexpression of rgs-CaM on salicylic acid signaling. Overexpressed and ectopically expressed rgs-CaM induced defense reactions, including cell death, generation of reactive oxygen species, and salicylic acid signaling. Further analysis using a combination of the salicylic acid analogue benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) and the Ca²⁺ ionophore A23187 revealed that rgs-CaM functions as an immune receptor that induces salicylic acid signaling by simultaneously perceiving both viral RSS and Ca²⁺ influx as infection cues, implying its autoactivation. Thus, secondary infection of SAR-induced tobacco plants with CMV seems to be effectively inhibited through 2b recognition and degradation by rgs-CaM, leading to reinforcement of antiviral RNA silencing and other salicylic acid-mediated antiviral responses.

IMPORTANCE Even without an acquired immune system like that in vertebrates, plants show enhanced whole-plant resistance against secondary infection with pathogens; this so-called systemic acquired resistance (SAR) has been known for more than half a century and continues to be extensively studied. SAR-induced plants strongly and rapidly express a number of antibiotics and pathogenesis-related proteins targeted against secondary infection, which can account for enhanced resistance against bacterial and fungal pathogens but are not thought to control viral infection. This study showed that enhanced resistance against cucumber mosaic virus is caused by a tobacco calmodulin-like protein, rgs-CaM, which detects and counteracts the major viral virulence factor (RNA silencing suppressor) after SAR induction. rgs-CaM-mediated SAR illustrates the growth versus defense trade-off in plants, as it targets the major virulence factor only under specific biotic stress conditions, thus avoiding the cost of constitutive activation while reducing the damage from virus infection.

植物病原体的初次感染通常会通过过敏反应引起水杨酸在植物中的大量积累，从而增强了对包括病毒在内的多种病原体的继发感染的抵抗力。这种现象称为系统获得性抗药性（SAR），这是一种植物适应反复的生物胁迫的启动剂。但是，SAR介导的抑制作用，尤其是病毒感染的抑制作用的分子机制仍不清楚。在这里，我们显示了针对烟草植物中的黄瓜花叶病毒（CMV）的SAR（烟草））涉及钙调蛋白样蛋白rgs-CaM。我们以前曾报道过rgs-CaM的抗病毒功能，该功能通过自噬作用结合并指导病毒RNA沉默抑制剂（RSSs）包括CMV 2b的降解。我们发现在正常生长的烟草植物中，rgs-CaM介导的免疫对CMV感染无效，但由于通过水杨酸信号引起的SAR诱导而被激活。然后，我们分析了rgs-CaM过表达对水杨酸信号传导的影响。过度表达和异位表达的rgs-CaM诱导防御反应，包括细胞死亡，活性氧的产生和水杨酸信号传导。使用水杨酸类似物苯并-（1,2,3）-噻二唑-7-硫代甲酸S-甲酯（BTH）和Ca ²⁺的组合进行进一步分析离子载体A23187揭示rgs-CaM可以作为一种免疫受体，通过同时感知病毒RSS和Ca ^2+的大量涌入作为感染线索，从而诱导水杨酸信号传导，暗示其自动激活。因此，rgs-CaM通过2b识别和降解似乎可以有效抑制SAR诱导的烟草植物CMV的继发感染，从而增强抗病毒RNA沉默和其他水杨酸介导的抗病毒反应。

重要性即使没有像脊椎动物那样的获得性免疫系统，植物也表现出增强的全株抗病原体继发感染的能力。这种所谓的系统获得性抵抗力（SAR）已经有半个多世纪的历史了，并且将继续得到广泛的研究。SAR诱导的植物强烈而快速地表达了许多针对继发感染的抗生素和与病程相关的蛋白，这些蛋白可以解释对细菌和真菌病原体的增强抗性，但不能控制病毒感染。这项研究表明，对黄瓜花叶病毒的抗性增强是由烟草钙调蛋白样蛋白rgs-CaM引起的，该蛋白检测并抵消SAR诱导后的主要病毒毒力因子（RNA沉默抑制剂）。