A salivary protein NlSP2 engages the OsCBSX3-SNAC3 module to enhance rice immunity.

Abstract

The molecular dialogue between rice and the brown planthopper (BPH; <i>Nilaparvata lugens</i>) is mediated by insect salivary effectors, yet the molecular mechanisms underlying plant perception and immune activation remain largely unclear. Here, we characterized the BPH salivary protein NlSP2, which is secreted into rice tissues during feeding. Silencing of <i>NlSP2</i> in BPH impairs salivary sheath formation, feeding ability, and survival, whereas its ectopic expression in rice enhances resistance to BPH via MAPK activation, H₂O₂ accumulation, and induction of defense-related genes. We identify the rice cystathionine β-synthase domain-containing protein OsCBSX3 as a direct intracellular target of NlSP2. Genetic analyses establish OsCBSX3 as a positive regulator of BPH resistance and an essential component of NlSP2-triggered immunity. NlSP2 binding promotes OsCBSX3 nuclear accumulation. In the nucleus, OsCBSX3 interacts with the NAC transcription factor SNAC3; NlSP2 enhances this interaction and potentiates SNAC3-mediated transcriptional activation of defense genes. Loss of <i>SNAC3</i> compromises rice resistance to BPH. Together, our results elucidate a complete signaling pathway linking insect effector perception to defense gene activation and highlight the OsCBSX3-SNAC3 module as a key regulator of rice immunity, providing insights into plant-insect interactions and potential targets for breeding resistant crops.