The salivary effector protein Sg2204 in the greenbug <i>Schizaphis graminum</i> suppresses wheat defence and is essential for enabling aphid feeding on host plants

Abstract

Aphids secrete diverse repertoires of salivary effectors into host plant cells to promote infestation by modulating plant defence. The greenbug Schizaphis graminum is an important cereal aphid worldwide. However, the secreted effectors of S. graminum are still uncharacterized. Here, 76 salivary proteins were identified from the watery saliva of S. graminum using transcriptome and proteome analyses. Among them, a putative salivary effector Sg2204 was significantly up-regulated during aphid feeding stages, and transient overexpression of Sg2204 in Nicotiana benthamiana inhibited cell death induced by BAX or INF1. Delivering Sg2204 into wheat via the type III secretion system of Pseudomonas fluorescens EtAnH suppressed pattern-triggered immunity (PTI)-associated callose deposition. The transcript levels of jasmonic acid (JA)- and salicylic acid (SA)-associated defence genes of wheat were significantly down-regulated, and the contents of both JA and SA were also significantly decreased after delivery of Sg2204 into wheat leaves. Additionally, feeding on wheat expressing Sg2204 significantly increased the weight and fecundity of S. graminum and promoted aphid phloem feeding. Sg2204 was efficiently silenced via spray-based application of the nanocarrier-mediated transdermal dsRNA delivery system. Moreover, Sg2204-silenced aphids induced a stronger wheat defence response and resulted in negative impacts on aphid feeding behaviour, survival and fecundity. Silencing of Sg2204 homologues from four aphid species using nanocarrier-delivered dsRNA also significantly reduced aphid performance on host plants. Thus, our study characterized the salivary effector Sg2204 of S. graminum involved in promoting host susceptibility by suppressing wheat defence, which can also be regarded as a promising RNAi target for aphid control.