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.

In flowering plants, hundreds of RNA editing events occur in the chloroplasts and mitochondria during post-transcriptional processes. Although several pentatricopeptide repeat (PPR) proteins have been shown to form the editosome core, the precise interactions between the different editing factors are still obscure. Here, we isolated an Arabidopsis (Arabidopsis thaliana) PPR protein, designated DELAYED GREENING409 (DG409), that was dually targeted to chloroplasts and mitochondria. This protein consists of 409 amino acids with seven PPR motifs but lacks a C-terminal E, E + or DYW domain. A mild dg409 knockdown mutant displays a sickly phenotype. In this mutant, the young leaves are pale green and turn green at maturity, and the development of chloroplasts and mitochondria is severely disrupted. Complete loss of DG409 function results in defective embryos. Transcriptomic analysis of the dg409 knockdown plants showed some editing defects in genes from both organelles, including CASEINOLYTIC PROTEASE P (clpP)-559, RNA POLYMERASE SUBUNIT ALPHA (rpoA)-200, ACETYL-COA CARBOXYLASE CARBOXYL TRANSFERASE SUBUNIT BETA (accD)-1568, NADH DEHYDROGENASE SUBUNIT 7 (nad7)-1505 and RIBOSOMAL PROTEIN S3 (rps3)-1344. RNA immunoprecipitation (RIP) showed that DG409 was associated with the targeted transcripts in vivo. Interaction assays revealed that DG409 directly interacted with two DYW-type PPR proteins [EARLY CHLOROPLAST BIOGENESIS2 (AtECB2) and DYW DOMAIN PROTEIN2 (DYW2)] and three multiple organellar RNA editing factors (MORF2, MORF8 and MORF9). These results indicate that DG409 is involved in RNA editing via protein complexes and is therefore essential for chloroplast and mitochondrial development.

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.