Insect-derived long non-coding RNAs function as epigenetic effectors to reprogram plant immunity

Abstract

Cross-kingdom RNAs are emerging as critical mediators of interspecies interactions, yet the functions of long RNAs such as mRNAs and long non-coding RNAs (lncRNAs) in recipient organisms remain largely unexplored. Here, we show that the brown planthopper (Nilaparvata lugens, BPH), a major rice pest, translocates mRNAs and lncRNAs into rice plants, where they migrate systemically from feeding sites to distal tissues. Compared with BPH mRNAs, BPH Salivary gland Cross-kingdom LncRNA (BSCLs) exhibit markedly higher stability in rice. Among them, BSCL1 functions as a virulence factor that promotes BPH feeding and reproduction by suppressing host defense. Mechanistically, BSCL1 associates with the HIRA histone chaperone complex and displaces histone H3.3 from the promoters of transcription factors, including bHLH genes central to jasmonic acid signaling, thereby repressing transcriptional immunity. Our results identify BSCLs as systemic, RNA-based effectors that reprogram host defense at the epigenetic level, revealing a previously unrecognized mode of insect-mediated manipulation of plant immunity and highlighting lncRNAs as cross-kingdom regulators. Significance StatementPlant-herbivore interactions are traditionally viewed as battles over nutrients and defense signaling, mediated largely by proteins and small RNAs. Here, we demonstrate that long non-coding RNAs from brown planthopper saliva are translocated into rice, migrate systemically, and function as epigenetic effectors that suppress key transcription factors in jasmonic acid-mediated defense. Unlike insect mRNAs, these lncRNAs persist in the plant and reprogram immunity by interfering with histone deposition. This discovery uncovers a new class of mobile, RNA-based virulence factors, expands our understanding of cross-kingdom regulation, and suggests innovative strategies for pest control targeting RNA effectors.