Herbivorous insects independently evolved salivary effectors to regulate plant immunity by destabilizing the malectin-LRR RLP NtRLP4

Plants rely on receptor-like proteins and receptor-like kinases (RLPs/RLKs) to detect a variety of invading pathogens and insects. However, it remains unclear how these invaders are able to overcome receptor perception and disable the plant signaling pathways. Here, we show that whiteflies and planthoppers independently evolve salivary effectors to target defensive RLP4, therefore minimizing the plant immunity. RLP4 is a leucine-rich repeat RLP (LRR-RLP) that confers plant resistance against herbivorous insects by forming RLP4/SOBIR1 complexes. In whitefly Bemisia tabaci , BtRDP is an Aleyrodidae-restricted protein that attaches to salivary sheath. It interacts with RLP4 from different plants, causing the degradation of RLP4 in an ubiquitin-dependent manner. Transgenic plants overexpressing NtRLP4 exerts a detrimental impact on B. tabaci by exploiting the crosstalk between the salicylic acid (SA) and jasmonic acid (JA) pathways. Conversely, the overexpression of BtRDP or silencing of NtRLP4 effectively alleviates such negative effects. In planthopper Nilaparvata lugens , a Delphacidae-restricted salivary protein NlSP694 also targets and promotes degradation of OsRLP4 from rice plants. Our results reveal the convergent evolution of salivary proteins in insects, and shed lights on the complex interactions between plants and herbivorous insects.