Opposing Roles of Foliar and Glandular Trichome Volatile Components in Cultivated Nightshade Interaction with a Specialist Herbivore

Plant chemistry is an important contributor to the interaction with herbivores. Here, we report on a previously unknown role for foliar and glandular trichome volatiles in their interaction with the specialist herbivore of solanaceous plants, the tomato red spider mite Tetranychus evansi. We used various bioassays and chemical analyses including coupled gas chromatography-mass spectrometry (GC/MS) and liquid chromatography coupled to quadrupole time of flight mass spectrometry (LC-QToF-MS) to investigate this interaction between cultivated African nightshades and T. evansi. We show that, whereas morphologically different cultivated African nightshade species released similar foliar volatile organic compounds (VOCs) that attracted T. evansi, VOCs released from exudates of ruptured glandular trichomes of one nightshade species influenced local defense on the leaf surface. VOCs from ruptured glandular trichomes comprising mainly saturated and unsaturated fatty acids deterred T. evansi oviposition. Of the fatty acids, the unsaturated fatty acids accounted for >40% of the oviposition deterrent activity. Our findings point to a defense strategy in a plant, based on opposing roles for volatiles released by foliar and glandular trichomes in response to attack by a specialist herbivore.

植物化学物质是介导植物与植食性昆虫互作的重要调控因子。本研究报道了叶毛与腺毛释放的挥发性物质在与茄科植物专食性天敌——番茄红蜘蛛螨（Tetranychus evansi）互作中的全新功能。我们通过多种生物测定法与化学分析手段——包括气相色谱-质谱联用（GC/MS）与液相色谱-四极杆飞行时间质谱（LC-QToF-MS）——探究了栽培型非洲茄属植物与番茄红蜘蛛螨之间的互作关系。研究结果显示：尽管形态各异的栽培非洲茄属物种释放的叶片挥发性有机化合物（VOCs）能够吸引番茄红蜘蛛螨，但其中一个茄属物种的破裂腺毛分泌物所释放的挥发性物质，可调控叶片表面的局部防御反应。以饱和脂肪酸与不饱和脂肪酸为主要成分的破裂腺毛挥发性物质，能够驱避番茄红蜘蛛螨产卵；其中不饱和脂肪酸贡献了超过40%的产卵驱避活性。本研究结果揭示了一种植物防御策略：其通过叶毛与腺毛释放的挥发性物质在响应专食性植食昆虫侵害时发挥截然相反的调控作用。