The salivary effector protein Sg2204 in the greenbug Schizaphis graminum 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.

Silencing an aphid-specific gene SmDSR33 for aphid control through plant-mediated RNAi in wheat

“…The signal peptide of Sm9723 was constituted of the first 21 amino acids and the cleavage site was predicted between residues 21 and 22 ( Zhang et al., 2022a ). The signal peptide of Sg2204 was constituted of the first 25 amino acids and the cleavage site was predicted between residues 25 and 26 ( Zhang et al., 2022b ).…”

“…M. persicae exhibited different feeding behaviors on nuclear-mediated RNAi transgenic plants and transplastomic-mediated RNAi transgenic plants ( Dong et al., 2022 ). Feeding behavior of S. miscanthi and S. graminum were significantly impaired after knockdown of Sm9723 and Sg2204 ( Zhang et al., 2022a ; Zhang et al., 2022b ).…”

“…Similarly, Sg2204 -silenced aphids exhibited a strong wheat defense response and negatively impacted aphid survival rate, fecundity, and feeding behavior. The aphid performance on host plants was significantly reduced when silencing the homologs of Sg2204 from four other aphid species ( Zhang et al., 2022a ; Zhang et al., 2022b ). These results implied that the genes encoding salivary proteins in aphids are potential candidates for aphid control in plants though plant-mediated RNAi.…”

Transcriptomic and proteomic analyses provide insights into host adaptation of a bamboo-feeding aphid

“…The glucose dehydrogenase belongs to the GMC oxidoreductase family and members of this family were shown to be present in caterpillar saliva most likely suppressing plant defenses by transcript regulation ( Bede et al., 2006 ). Glucose dehydrogenase has been previously characterized in several other aphids, such as the A. pisum ( Carolan et al., 2011 ), Diuraphis noxia ( Nicholson et al., 2012 ), S. graminum ( Zhang et al., 2022 ), S. avenae ( Zhang et al., 2017 ), M. euphorbiae ( Chaudhary et al., 2015 ), Metopolophium dirhodum ( Rao et al., 2013 ) and Schlechtendalia chinensis ( Yang et al., 2018 ). The dramatically overexpression of this gene in the P. bambucicola salivary glands may indicate that it also plays an important role in P. bambucicola feeding and adaption to bamboo.…”

“…Salivary sugar degrading enzymes, peptidases and proteases in insects can function as important digestive enzymes degrading plant polysaccharide and plant defense proteins ( Nicholson et al., 2012 ; Liu et al., 2016 ; Zhang et al., 2017 ). Some digestive enzymes detected in P. bambucicola salivary gland or saliva secretomes have been also found in salivary gland or saliva of some aphids and other phloem-feeding insects, such as the lysosomal alpha-mannosidase ( Wu et al., 2021 ), carboxypeptidase ( Huang et al., 2020 ), cathepsin ( Foissac et al., 2002 ; Zhang et al., 2017 ; Huang et al., 2020 ; Wu et al., 2021 ; Zhang et al., 2022 ), serine protease ( Nicholson et al., 2012 ; Zhang et al., 2017 ) and phospholipase ( Zhang et al., 2017 ). These putative secretory effectors may be essential for enabling P. bambucicola feeding on bamboo host, such as helping promote aphid stylet penetration, digestion and detoxification of toxins, or suppressing plant defenses against P. bambucicola .…”