Plants deploy receptor-like kinases and nucleotide-binding leucine-rich repeat receptors to confer host plant resistance (HPR) to herbivores¹. These gene-for-gene interactions between insects and their hosts have been proposed for more than 50 years². However, the molecular and cellular mechanisms that underlie HPR have been elusive, as the identity and sensing mechanisms of insect avirulence effectors have remained unknown. Here we identify an insect salivary protein perceived by a plant immune receptor. The BPH14-interacting salivary protein (BISP) from the brown planthopper (Nilaparvata lugens Stål) is secreted into rice (Oryza sativa) during feeding. In susceptible plants, BISP targets O. satvia RLCK185 (OsRLCK185; hereafter Os is used to denote O. satvia-related proteins or genes) to suppress basal defences. In resistant plants, the nucleotide-binding leucine-rich repeat receptor BPH14 directly binds BISP to activate HPR. Constitutive activation of Bph14-mediated immunity is detrimental to plant growth and productivity. The fine-tuning of Bph14-mediated HPR is achieved through direct binding of BISP and BPH14 to the selective autophagy cargo receptor OsNBR1, which delivers BISP to OsATG8 for degradation. Autophagy therefore controls BISP levels. In Bph14 plants, autophagy restores cellular homeostasis by downregulating HPR when feeding by brown planthoppers ceases. We identify an insect saliva protein sensed by a plant immune receptor and discover a three-way interaction system that offers opportunities for developing high-yield, insect-resistant crops.

Summary: The planthopper resistance gene Bph6 encodes a protein that interacts with OsEXO70E1. EXO70 forms a family of paralogues in rice. We hypothesized that the EXO70‐dependent trafficking pathway affects the excretion of resistance‐related proteins, thus impacting plant resistance to planthoppers. Here, we further explored the function of EXO70 members in rice resistance against planthoppers. We used the yeast two‐hybrid and co‐immunoprecipitation assays to identify proteins that play roles in Bph6‐mediated planthopper resistance. The functions of the identified proteins were characterized via gene transformation, plant resistance evaluation, insect performance, cell excretion observation and cell wall component analyses. We discovered that another EXO70 member, OsEXO70H3, interacted with BPH6 and functioned in cell excretion and in Bph6‐mediated planthopper resistance. We further found that OsEXO70H3 interacted with an S‐adenosylmethionine synthetase‐like protein (SAMSL) and increased the delivery of SAMSL outside the cells. The functional impairment of OsEXO70H3 and SAMSL reduced the lignin content and the planthopper resistance level of rice plants. Our results suggest that OsEXO70H3 may recruit SAMSL and help its excretion to the apoplast where it may be involved in lignin deposition in cell walls, thus contributing to rice resistance to planthoppers.

Rice (Oryza sativa L.) is the staple food of more than half of Earth’s population. Brown planthopper (Nilaparvata lugens Stål, BPH) is a host-specific pest of rice responsible for inducing major losses in rice production. Utilizing host resistance to control N. lugens is considered to be the most cost-effective method. Therefore, the exploration of resistance genes and resistance mechanisms has become the focus of breeders’ attention. During the long-term co-evolution process, rice has evolved multiple mechanisms to defend against BPH infection, and BPHs have evolved various mechanisms to overcome the defenses of rice plants. More than 49 BPH-resistance genes/QTLs have been reported to date, and the responses of rice to BPH feeding activity involve various processes, including MAPK activation, plant hormone production, Ca²⁺ flux, etc. Several secretory proteins of BPHs have been identified and are involved in activating or suppressing a series of defense responses in rice. Here, we review some recent advances in our understanding of rice–BPH interactions. We also discuss research progress in controlling methods of brown planthoppers, including cultural management, trap cropping, and biological control. These studies contribute to the establishment of green integrated management systems for brown planthoppers.

Cold damage is one of the most important environmental factors influencing crop growth, development, and production. In this study, we generated a pair of near-isogenic lines (NILs), Towada and ZL31, and Towada showed more cold sensitivity than ZL31 in the rice seedling stage. To explore the transcriptional regulation mechanism and the reason for phenotypic divergence of the two lines in response to cold stress, an in-depth comparative transcriptome study under cold stress was carried out. Our analysis uncovered that rapid and high-amplitude transcriptional reprogramming occurred in the early stage of cold treatment. GO enrichment and KEGG pathway analysis indicated that genes of the response to stress, environmental adaptation, signal transduction, metabolism, photosynthesis, and the MAPK signaling pathway might form the main part of the engine for transcriptional reprogramming in response to cold stress. Furthermore, we identified four core genes, OsWRKY24, OsCAT2, OsJAZ9, and OsRR6, that were potential candidates affecting the cold sensitivity of Towada and ZL31. Genome re-sequencing analysis between the two lines revealed that only OsWRKY24 contained sequence variations which may change its transcript abundance. Our study not only provides novel insights into the cold-related transcriptional reprogramming process, but also highlights the potential candidates involved in cold stress.

The brown planthopper (BPH; Nilaparvata lugens Stål) is the most significant insect pest compromising rice production globally. Phytohormones, which are small organic compounds produced by plants, play a crucial role in regulating plant growth and development. Nevertheless, extensive research has established that phytohormones are essential in modulating plant defense against BPH. Plants can achieve equilibrium between growth and defense by utilizing the intricate network of phytohormone signaling pathways to initiate optimal and efficient defensive responses to insects. In this review, we primarily address the roles of phytohormones in conferring resistance against BPH, with a focus on hormone cross-talk. We also discuss the potential value of integrating hormones with other agricultural practices to enhance plant defense and agricultural yield, which highlights the significance of novel approaches for environment-friendly insect pest management.