Salivary Glucose Oxidase from Caterpillars Mediates the Induction of Rapid and Delayed-Induced Defenses in the Tomato Plant

Caterpillars produce oral secretions that may serve as cues to elicit plant defenses, but in other cases these secretions have been shown to suppress plant defenses. Ongoing work in our laboratory has focused on the salivary secretions of the tomato fruitworm, Helicoverpa zea. In previous studies we have shown that saliva and its principal component glucose oxidase acts as an effector by suppressing defenses in tobacco. In this current study, we report that saliva elicits a burst of jasmonic acid (JA) and the induction of late responding defense genes such as proteinase inhibitor 2 (Pin2). Transcripts encoding early response genes associated with the JA pathway were not affected by saliva. We also observed a delayed response to saliva with increased densities of Type VI glandular trichomes in newly emerged leaves. Proteomic analysis of saliva revealed glucose oxidase (GOX) was the most abundant protein identified and we confirmed that it plays a primary role in the induction of defenses in tomato. These results suggest that the recognition of GOX in tomato may represent a case for effector-triggered immunity. Examination of saliva from other caterpillar species indicates that saliva from the noctuids Spodoptera exigua and Heliothis virescens also induced Pin2 transcripts.

植食性毛虫（caterpillars）分泌的口腔分泌物可作为触发植物防御反应的信号，但在部分情境中，此类分泌物业已被证实能够抑制植物的防御机制。本实验室目前的研究工作聚焦于番茄果蛀虫（Helicoverpa zea）的唾液分泌物。既往研究中，我们已证实其唾液及其主要成分葡萄糖氧化酶（glucose oxidase）可作为效应因子，抑制烟草的防御反应。在本研究中，我们发现唾液可诱导茉莉酸（jasmonic acid, JA）爆发式积累，并上调晚期响应防御基因的表达，例如蛋白酶抑制剂2（proteinase inhibitor 2, Pin2）。与茉莉酸通路相关的早期响应基因的转录本水平不受唾液影响。我们还观察到，新生叶片的VI型腺毛（Type VI glandular trichomes）密度随唾液处理后延迟升高，呈现对唾液的延迟响应。对唾液的蛋白质组学分析显示，葡萄糖氧化酶（glucose oxidase, GOX）是所鉴定出的丰度最高的蛋白，我们证实其在番茄防御反应的诱导中发挥核心作用。上述结果表明，番茄对葡萄糖氧化酶的识别或许属于效应因子触发免疫（effector-triggered immunity）的典型案例。对其他毛虫物种唾液的检测显示，夜蛾科（noctuids）的甜菜夜蛾（Spodoptera exigua）和烟芽夜蛾（Heliothis virescens）的唾液同样可诱导Pin2基因的转录。