A salivary sheath protein essential for the interaction of the brown planthopper with rice plants.
Salivary secretions, including gel saliva and watery saliva, play crucial roles in the interaction between the insect and plant during feeding. In this study, we identified a salivary gland-specific gene encoding a salivary sheath protein (NlShp) in Nilaparvata lugens. NlShp has two alternative splicing variants; both are expressed at high levels during the nymph and adult stages. Immunohistochemical staining showed that the NlShp were synthesized in the principal gland cells of the salivary gland. LC-MS/MS and western blot analysis confirmed that NlShp was one of the components of the salivary sheath. Simultaneously knocking down the two NlShp variants by RNA interference inhibited both salivary ﬂange and salivary sheath formation and resulted in a lethal phenotype within four days for the brown planthopper (BPH) feeding on rice plants, indicating that the salivary sheath and salivary ﬂanges were essential for plant-associated feeding. Despite the salivary sheath deficiency, no obvious phenotype was observed in the NlShp-knockdown BPHs fed on artificial diet. The electrical penetration graph (EPG) results showed that salivary sheath-deficient BPHs exhibited a prolonged nonpenetration period, scarce sap period, and increased stylet movement on rice plants and eventually starved to death. Our results provided evidence that the interaction between the salivary sheath and host plant might be a critical step in successful BPH feeding. According to present research, we propose a salivary sheath required feeding model for piercing-sucking insects and provide a potential target for rice planthopper management.
State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou, 310058, China.
Hai-Jian
HJ
Huang
State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou, 310058, China.
Cheng-Wen
CW
Liu
State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou, 310058, China.
Ye-Fang
YF
Cai
State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou, 310058, China.
Min-Zhu
MZ
Zhang
State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou, 310058, China.
Yan-Yuan
YY
Bao
State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou, 310058, China. Electronic address: chxzhang@zju.edu.cn.
Chuan-Xi
CX
Zhang
D017398:Alternative Splicing; D000818:Animals; D005247:Feeding Behavior; D006430:Hemiptera / Q000737:chemistry / Q000235:genetics*; D019476:Insect Proteins / Q000235:genetics; D009758:Nymph / Q000737:chemistry / Q000235:genetics; D012275:Oryza / Q000469:parasitology*; D034622:RNA Interference; D012463:Saliva / Q000737:chemistry*; D012469:Salivary Glands / Q000378:metabolism*
D019476:Insect Proteins
EPG; Feeding; Host interaction; Nilaparvata lugens; RNA interference; Salivary sheath protein