SmCSP4 from aphid saliva stimulates salicylic acid‐mediated defence responses in wheat by interacting with transcription factor TaWKRY76

Abstract

SummaryAphid salivary proteins are critical in modulating plant defence responses. Grain aphid Sitobion miscanthi is an important wheat pest worldwide. However, the molecular basis for the regulation of the plant resistance to cereal aphids remains largely unknown. Here, we show that SmCSP4, a chemosensory protein from S. miscanthi saliva, is secreted into wheat plants during aphid feeding. Delivery of SmCSP4 into wheat leaves activates salicylic acid (SA)‐mediated plant defence responses and subsequently reduces aphid performance by deterring aphid feeding behaviour. In contrast, silencing SmCSP4 gene via nanocarrier‐mediated RNAi significantly decreases the ability of aphids to activate SA defence pathway. Protein–protein interaction assays showed that SmCSP4 directly interacts with wheat transcriptional factor TaWRKY76 in plant nucleus. Furthermore, TaWRKY76 directly binds to the promoter of SA degradation gene Downy Mildew Resistant 6 (DMR6) and regulates its gene expression as transcriptional activator. SmCSP4 secreted by aphids reduces the transcriptional activation activity of TaWRKY76 on DMR6 gene expression, which is proposed to result in increases of SA accumulation and enhanced plant immunity. This study demonstrated that SmCSP4 acts as salivary elicitor that is involved in activating SA signalling defence pathway of wheat by interacting with TaWRKY76, which provide novel insights into aphid‐cereal crops interactions and the molecular mechanism on induced plant immunity.

Roles of herbivorous insects salivary proteins

“…During S. miscanthi feeding, the application of Sm10 or SmC002 into wheat plants significantly inhibits callose deposition and alters the transcript levels of callose synthase genes [ 70 ]. Additionally, SmCSP4, secreted into wheat plants during S. miscanthi feeding, activates the SA-mediated defense pathway; silencing the SmCSP4 gene diminishes the aphids' ability to activate the SA defense pathway [ 71 ]. The salivary protein Cathepsin B3 from Myzus persicae (Diptera, Culicidae) elicits a recognition response in Nicotiana tabacum plants, resulting in the suppression of aphid feeding through the accumulation of reactive oxygen species (ROS) [ 72 ].…”