Gao Haoli, Zou Jianzheng, Lin Xumin, Zhang Huihui, Yu Na, Liu Zewen
Key laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Weigang 1, Nanjing 210095, China.
J Exp Bot. 2022 Dec 8;73(22):7477-7487. doi: 10.1093/jxb/erac354.
The brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), is a serious insect pest on rice. It uses its stylet to collect sap by penetrating the phloem and at the same time it delivers saliva into the host plant, which can trigger a reaction. The molecular mechanisms by which BPH salivary proteins result in plant responses are poorly understood. In this study, we screened transcriptomic data from different BPH tissues and found a protein specific to the salivary gland, NlG14, that could induce cell death in plants. We determined that NlG14 is uniquely found in the insect family Delphacidae. Detailed examination of N. lugens showed that NlG14 was mainly localized in the A-follicle of the principal gland of the salivary gland, and that it was secreted into rice plants during feeding. Knockdown of NlG14 resulted in significant nymph mortality when BPH was fed on either rice plants or on an artificial diet. Further analysis showed that NlG14 triggered accumulation of reactive oxygen species, cell death, callose deposition, and activation of jasmonic acid signaling pathways in plants. Transient expression of NlG14 in Nicotiana benthamiana decreased insect feeding and suppressed plant pathogen infection. Thus, NlG14, an essential salivary protein of N. lugens, acted as a potential herbivore-associated molecular pattern to enhance plant resistance to both insects and plant pathogens by inducing multiple plant defense responses. Our findings provide new insights into the molecular mechanisms of insect-plant interactions and offer a potential target for pest management.
褐飞虱（Nilaparvata lugens (Stål)，半翅目：飞虱科）是水稻上的一种严重害虫。它通过口针穿透韧皮部来吸取汁液，同时将唾液注入寄主植物，这可能引发植物的反应。目前对褐飞虱唾液蛋白引发植物反应的分子机制了解甚少。在本研究中，我们筛选了褐飞虱不同组织的转录组数据，发现了一种唾液腺特有的蛋白NlG14，它能诱导植物细胞死亡。我们确定NlG14仅在飞虱科昆虫中存在。对褐飞虱的详细检查表明，NlG14主要定位于唾液腺主腺的A滤泡中，并且在取食过程中会分泌到水稻植株中。敲低NlG14会导致褐飞虱若虫在取食水稻植株或人工饲料时出现显著死亡。进一步分析表明，NlG14会引发植物体内活性氧的积累、细胞死亡、胼胝质沉积以及茉莉酸信号通路的激活。在本氏烟草中瞬时表达NlG14会减少昆虫取食并抑制植物病原体感染。因此，NlG14作为褐飞虱一种必需的唾液蛋白，通过诱导多种植物防御反应，作为一种潜在的与植食性昆虫相关的分子模式，增强了植物对昆虫和植物病原体的抗性。我们的研究结果为昆虫 - 植物相互作用的分子机制提供了新的见解，并为害虫管理提供了一个潜在的靶点。
