蚜虫是世界范围内危害性最强的农业害虫之一，它们也是多种植物病毒的传播介体。被蚜虫取食的植物会产生充当信号分子的挥发性化合物，这些化合物释放到空气中后会被临近植物吸收并促使临近植物产生对蚜虫的抗性，这个现象被称为“气传性免疫”。虽然这种植物间交流及其生态学功能已在多种植物中被报道，但整个过程的分子机制和信号通路仍是未解之谜。本研究发现蚜虫取食会上调植物中水杨酸（SA）的水平，SA上调会增强转录因子NAC2的表达，NAC2能够结合SAMT1的启动子，促进SAMT1的表达，SAMT1能够将SA转化成水杨酸甲酯（MeSA），挥发至空气中。MeSA被临近植物通过SABP2识别并转化为SA。SA作为起始信号，促进临近植物中NAC2的表达，进而激活NAC2-SAMT1模块，促进临近植物产生MeSA去抵抗、趋避蚜虫。本研究还发现NAC2-SAMT1模块能够参与植物对CMV、PVY的基础抗性，MeSA介导的气传性免疫也能够抑制蚜虫在临近植物上的病毒传播过程。揭示了气传性免疫抗蚜虫及其传病毒的分子机制后，继续探索病毒是否存在针对植物气传性免疫的反防御机制。本研究发现黄瓜花叶病毒（CMV）编码的1a蛋白能够通过解旋酶结构域与NAC2互作，进而抑制NAC2的核定位，促进NAC2被26S蛋白酶体降解，从而抑制SAMT1的转录、影响MeSA的生成。之后构建了1aG983D突变体，发现突变体失去了与NAC2互作后，也失去了抑制气传免疫的功能。此外，本研究还发现蚜虫传播的马铃薯Y病毒（PVY）也能干扰MeSA的生成进而干扰植物气传免疫过程。和1a相似，PVY编码的CI蛋白也是通过解旋酶结构域与NAC2互作，抑制NAC2的核定位，而突变体CIG347D则在丧失互作功能后也丧失了影响NAC2的功能。因此，通过互作来抑制NAC2核定位、干扰NAC2对SAMT1的转录可能是蚜虫传病毒抑制植物气传性免疫的通用策略。这些研究结果预示着不仅病毒会利用蚜虫作为传播介体，蚜虫也会利用病毒去干扰植物气传免疫过程以利其更好地繁殖。这个植物-病毒博弈过程也为蚜虫和病毒共进化方面研究提供了新思路。综上所述，本研究从蚜虫、病毒、被取食植物、临近植物四个角度全面解析了气传性免疫分子机制，研究结果为充分利用植物产生的挥发性化合物作为生物武器帮助农作物更好地抵御昆虫的侵害和病毒的侵染提供了理论基础。
Aphids are the most destructive agricultural and horticultural pests worldwide. They can efficiently transmit many devastating viral pathogens. Aphid-attacked plants release volatile organic compounds （VOCs） as intra- and interplant signaling messengers. These VOCs released from stressed plants, so called VOC ‘emitter’ plants, can serve as aerial phytohormones and perceived by adjacent plants to elicit defense reactions in neighboring ‘receiver’ plants, a phenomenon known as airborne immunity （AI）. Such plant-plant communication （PPC） and its biological and ecological significance have been observed in many species for several decades. However, molecular and genetic framework for the intriguing AI remains an unknown mystery.In this study, we found that aphids feeding elicits salicylic acid （SA） response and increases SA level in attacked plants. The transcription factor NAC2 can be activated by upregulated SA level and directly bind to SAMT1 promoter, activating its transcription. SAMT1 then catalyzes SA to form airborne methyl salicylate （MeSA）. Airborne MeSA is then perceived and converted to SA by SABP2 in neighboring plants. Further, we found that intracellular SA serves as a cue to activate NAC2 expression, subsequently triggering NAC2-SAMT1 module to produce MeSA for aphid antixenosis. We also found that NAC2-SAMT1 module participates in plant basal antiviral defense against Cucumber mosaic virus （CMV） and Potato virus Y （PVY）. In addition, MeSA-mediated AI induces aphid antixenosis and suppresses virus transmission by aphids in neighboring receiver plants. Elucidation of the molecular insight into AI against aphids and viruses raises an intriguing question on whether and how virus counteracts AI and affects aphid survival in receiver plants. We found that helicase domain-containing CMV 1a protein could suppress AI through its interaction with NAC2 to partially change the subcellular localization of NAC2 from nuclei to cytoplasm, and to promote the NAC2 degradation via the 26S proteasome to block SAMT1 transcription and subsequent MeSA biosynthesis. We constructed mutant 1aG983D, which abolishes its interaction with NAC2 and biological functions in perturbing MeSA signaling and AI. Moreover, infection by PVY also suppresses MeSA volatilization from plants after aphid attack and negatively regulates AI against aphids and viruses. Similar to CMV 1a, the helicase domain-containing PVY CI, but not CIG347D interacts with NAC2 and alters the NAC2 localization. Therefore, aphid-transmitted viruses may generally use their helicase domain-containing proteins to suppress NAC2 transcription function and counteract AI in plants. These findings further suggest that not only viruses can utilize aphids as vector for transmission, but also aphids can in turn exploit viruses to facilitate their surviving and thriving in plants where AI is suppressed by viral proteins. This unexpected countermeasure reveals an undefined ecological and co-evolutionary mutualism between aphids and aphid-transmissible viruses.In summary, we have exploited interplays among aphid, virus, VOC emitter, and receiver plants in a qaudri-pathosystem to dissect AI. Deciphering AI lays the groundwork to empower VOCs as a novel bioinspired tool in defense of plants including agricultural and horticultural crops against insect infestation and virus epidermic.
