Reviewer #2 (Public review): Herbivorous insects independently evolved salivary effectors to regulate plant immunity by destabilizing the malectin-LRR RLP NtRLP4

Plants depend on receptor-like proteins and receptor-like kinases (RLPs/RLKs) to detect a variety of invading pathogens and insects. Although the mechanisms of microbial pathogens in suppressing plant immunity have been well investigated, it remains unclear how herbivorous insects overcome receptor-mediated defenses. Here, we show that salivary effectors evolve independently in whiteflies and planthoppers to target defensive RLP4, therefore minimizing the plant immunity. RLP4, as a leucine-rich repeat RLP (LRR-RLP), confers plant resistance against herbivorous insects by forming the RLP4/SOBIR1 complexes. In the whitefly Bemisia tabaci, BtRDP, the Aleyrodidae-specific salivary sheath protein, interacts with RLP4 from multiple plant species and promotes its ubiquitin-dependent degradation. Overexpression of NtRLP4 in transgenic plants exerts a detrimental impact on B. tabaci by exploiting the crosstalk between the salicylic acid (SA) and jasmonic acid (JA) pathways. Conversely, overexpression of BtRDP or silencing of NtRLP4 effectively alleviates such negative effects. In planthopper Nilaparvata lugens, the Delphacidae-restricted salivary protein NlSP104 also targets and promotes the degradation of OsRLP4 from rice plants. Our results reveal the convergent evolution of salivary proteins in insects, and highlight the complex interactions between plants and herbivorous insects.