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The brown planthopper (BPH) Nilaparvata lugens (Stål) is a main pest on rice. It secretes saliva to regulate plant defense responses, when penetrating rice plant and sucking phloem sap through its stylet. However, the molecular mechanisms of BPH salivary proteins regulating plant defense responses remain poorly understood. A N. lugens DNAJ protein (NlDNAJB9) gene was highly expressed in salivary glands, and the knock down of NlDNAJB9 significantly enhanced honeydew excretion and fecundity of the BPH. NlDNAJB9 could induce plant cell death, and the overexpression of NlDNAJB9 gene in Nicotiana benthamiana induced calcium signaling, mitogen-activated protein kinase (MAPK) cascades, reactive oxygen species (ROS) accumulation, jasmonic acid (JA) hormone signaling and callose deposition. The results from different NlDNAJB9 deletion mutants indicated that the nuclear localization of NlDNAJB9 was not necessary to induce cell death. The DNAJ domain was the key region to induce cell death, and the overexpression of DNAJ domain in N. benthamiana significantly inhibited insect feeding and pathogenic infection. NlDNAJB9 might interact indirectly with NlHSC70-3 to regulate plant defense responses. NlDNAJB9 and its orthologs were highly conserved in three planthopper species, and could induce ROS burst and cell death in plants. Our study provides new insights into the molecular mechanisms of insect-plant interactions. [ABSTRACT FROM AUTHOR]

Saliva plays important roles in insect feeding, but its roles in insect reproduction were rarely reported. Here we reported that the knockdown of a salivary gland-specific gene NlG14 disrupted the reproduction through inhibiting the ovulation of the brown planthopper (BPH), Nilaparvata lugens (Stål), one of the most devastating rice pests in Asia. NlG14 knockdown caused the displacement of the lateral oviduct secreted components (LOSC), leading to the ovulation disorder and the accumulation of mature eggs in the ovary. The RNAi-treated females laid much less eggs than their control counterparts, though they had the similar oviposition behavior on rice stems as controls. NlG14 protein was not secreted into the hemolymph, indicating an indirect effect of NlG14 knockdown on BPH reproduction. NlG14 knockdown caused the malformation of A-follicle of the principal gland and affected the underlying endocrine mechanism of salivary glands. NlG14 reduction might promote the secretion of insulin-like peptides NlILP1 and NlILP3 from the brain, which up-regulated the expression of Nllaminin gene and then caused the abnormal contraction of lateral oviduct muscle. Another explanation was NlG14 reduction disrupted the ecdysone biosynthesis and action through the insulin-PI3K-Akt signaling in ovary. Altogether, this study indicated that the salivary gland specific protein NlG14 indirectly mediated BPH ovulation process, which established a connexon in function between insect salivary gland and ovary. Author summary: Salivary glands play important roles in the feeding process of animals. The salivary glands of insects can secrete various proteins through the exocrine pathway to help them digest and regulate the defense response of host. The endocrine function of insect salivary glands is rarely reported. We found that decreased expression of the salivary protein gene NlG14 resulted in abnormal contraction of lateral oviduct muscles, thus inhibiting ovulation of the brown planthopper. NlG14 could not be secreted into the haemolymph as an endocrine function, but NlG14 knockdown caused the deformity of salivary gland. The reduction of NlG14 regulated insulin release in the brain and insulin-PI3K-Akt signaling in ovary. The disruption of these signaling pathways caused the abnormal contraction of lateral oviduct muscles, resulting in ovulation disorders. These findings provide a case of salivary gland regulating ovarian reproduction in insects. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]