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.

Gene order and location in chromosomes of species are non-random. Neighboring gene pairs tend to display some similarities, such as co-expression and co-modification. However, the contribution of linear proximity, spatial proximity, and evolutionary proximity to these similarities remain unclear, together with whether the presence of several types of proximity can strengthens the similarities. In this study, we investigated the properties of three kinds of colocalized gene pairs: intrachromosomal colocalized gene pairs, always-neighboring gene pairs, and evolutionary neighboring gene pairs. Our analysis showed that (1) Different types of colocalized genes differentially contribute to co-expression, co-modifications and conservation across species; (2) Intrachromosomal colocalization can strengthen co-expression and co-modification of neighboring gene pairs and their conservation across species; (3) The combination of the three kinds of colocalization can lead to the strongest co-modification and is most strongly conserved across species. (4) Colocalized gene pairs are indicative of phylogenetic relationships and whole genome duplications (WGDs). These results provide valuable clues for future efforts to understand the characteristics of colocalized gene pairs and how the neighborhood affects their interactions.

Introduction: The brown planthopper (BPH) poses a significant threat to rice production in Asia. The use of resistant rice varieties has been effective in managing this pest. However, the adaptability of BPH to resistant rice varieties has led to the emergence of virulent populations, such as biotype Y BPH. YHY15 rice, which carries the BPH resistance gene Bph15, exhibits notable resistance to biotype 1 BPH but is susceptible to biotype Y BPH. Limited information exists regarding how resistant rice plants defend against BPH populations with varying levels of virulence.Methods: In this study, we integrated miRNA and mRNA expression profiling analyses to study the differential responses of YHY15 rice to both avirulent (biotype 1) and virulent (biotype Y) BPH.Results: YHY15 rice demonstrated a rapid response to biotype Y BPH infestation, with significant transcriptional changes occurring within 6 hours. The biotype Y-responsive genes were notably enriched in photosynthetic processes. Accordingly, biotype Y BPH infestation induced more intense transcriptional responses, affecting miRNA expression, defenserelated metabolic pathways, phytohormone signaling, and multiple transcription factors. Additionally, callose deposition was enhanced in biotype Y BPH-infested rice seedlings.Discussion: These findings provide comprehensive insights into the defense mechanisms of resistant rice plants against virulent BPH, and may potentially guide the development of insect-resistant rice varieties.

Secondary metabolites, resistance genes Insect herbivores and their host plants engage in a dynamic molecular conflict, wherein plants have evolved sophisticated defense mechanisms, while insects have developed strategies to suppress these defenses. These interactions involve intricate molecular processes that are a major focus of research, with the goal of improving pest control strategies.Herbivorous insects, such as piercing-sucking hemipterans and chewing Lepidopterans, establish close associations with host plants to manipulate plant cellular processes for feeding and reproduction (Erb and Reymond, 2019). In response, plants have evolved complex immune systems composed of signaling pathways, resistance genes, and secondary metabolites. This ongoing molecular arms race between plants and insects is characterized by interactions among a diverse array of molecules from both organisms. Plant secondary metabolites and resistance genes serve as defense mechanisms against insect herbivory, while insects utilize detoxification enzymes and effectors to disrupt plant defenses, enhancing their adaptation. This Research Topic explores the complex genetic, physical, metabolic, and molecular interactions between plants and insects, examined through advanced omics technologies such as genomics, transcriptomics, and metabolomics. The collection includes 16 original research and review articles focusing on herbivorous insects (e.g., brown planthopper, aphids, psyllids) and their host plants (e.g., rice, maize, cotton), which are summarized below.Eight articles in this collection (one review and seven research articles) focus on the interaction between rice (Oryza sativa L.) and the brown planthopper (Nilaparvata lugens Stål, BPH). This interaction serves as a valuable model system for studying the molecular mechanisms underlying plant-insect interactions. The brown planthopper is a major pest that causes significant damage to rice crops (Cheng et al., 2013;Jing et al., 2017), and the deployment of resistant rice varieties has proven effective in managing this pest. To date, over 40 resistance loci and 17 resistance genes for brown planthopper have been identified and functionally characterized (Shar et al., 2023).The molecular mechanisms of these resistance genes represent a key area of research. This issue includes articles on the molecular mechanisms involving four specific resistance genes: Bph6, Bph14, Bph15, and Bph30.Four articles focus on Bph15, examining the specific cells and tissues involved in resistance, the role of OsWRKY71 in Bph15-mediated resistance, the defense mechanisms against BPH populations with varying virulence levels, and transcriptomic analysis to elucidate the mechanisms behind BPH14/BPH15-conferred resistance. One article investigates how indole-3-acetic acid (IAA) negatively regulates Bph30-mediated resistance using combining transcriptomic and metabolomic analyses. Two additional articles (one review and one research) explore the impact of non-coding RNAs on the interaction between rice and brown planthopper, and one article identifies BPH resistance genes using Genome-wide association studies (GWAS) and evaluates the predictive ability of genomic selection for resistance to BPH. Two articles in this Research Topic examine aphids as vectors in tritrophic interactions. Zhao et al. investigate the effects of nitrogen fertilization on the emission of plant volatile organic compounds (VOCs) that mediate interactions among maize, aphids, and ladybirds. Specifically, 1-nonene was identified as a key compound attracting ladybirds, with its release positively correlated with the visitation rates of Harmonia axyridis. The study demonstrated that supplying 1-nonene to maize under low-nitrogen conditions increased the attractiveness of plants to ladybirds, highlighting the compound's role in tritrophic interactions. The synthesis of 1-nonene is linked to salicylic acid (SA) and abscisic acid (ABA), indicating complex interactions within plant response mechanisms to nutrient availability and pest infestation. This research enhances our understanding of plant metabolic responses to nutrient levels and offers practical insights for improving pest management and crop production.Pandey et al. explore the influence of host plants on the gene expression of the cotton aphid (Aphis gossypii Glover) when infected with the cotton leafroll dwarf virus (CLRDV). Using four host plants-cotton, hibiscus, okra, and prickly sida-the study revealed significant differences in gene expression among aphids acquiring the virus from different hosts. A total of 2,942 differentially expressed genes (DEGs) were identified, with varying DEG counts across hosts: 750 from cotton, 310 from hibiscus, 1,193 from okra, and 689 from prickly sida. Notably, more genes were overexpressed in aphids from cotton, hibiscus, and prickly sida, while more genes were underexpressed in aphids from okra. These findings underscore the complexity of vector-virus-host interactions and the pivotal role of host plants in influencing disease transmission.Two articles in this Research Topic focus on psyllids as vectors in vector-pathogen interactions. Li et al. examine the biochemical effects of Candidatus Liberibacter solanacearum (CLso) infection in potato psyllids (Bactericera cockerelli), vectors of diseases such as psyllid yellows, vein-greening (VG), and zebra chip (ZC).Using ultra-performance liquid chromatography tandem mass spectrometry (UPLC-MS/MS), the study identified 34 metabolites related to amino acid, carbohydrate, and lipid metabolism as potential biomarkers of CLso infection.Matrix-assisted Laser Desorption Ionization Mass Spectrometry Imaging (MALDI-MSI) mapped the spatial distribution of these biomarkers, revealing significant down-regulation of 15-keto-Prostaglandin E2 and alpha-D-Glucose in the abdomen of infected psyllids. These findings suggest mechanisms of immune suppression employed by CLso to...

The Cleavage Stimulation Factor (CstF) complex, consisting of three subunits, is essential for the 3′ end processing of precursor messenger RNA (pre-mRNA). In mammals, this complex includes CstF50, CstF64, and CstF77, named according to their molecular weights, and these proteins are conserved across many organisms. However, the functional roles of the three CstF genes (NlCstF50, NlCstF64, and NlCstF77) in Nilaparvata lugens, a major rice pest, have not been fully explored. This study identified and characterized the sequences of these genes, with proteins encoded by NlCstF50, NlCstF64, and NlCstF77 consisting of 439, 419, and 732 amino acids, respectively. These proteins are conserved among various insect species. Spatio-temporal expression analysis revealed that these genes are expressed at all developmental stages and in various tissues, with peak levels in eggs and testes. RNA interference (RNAi) targeting one or all three NlCstF genes resulted in a reduction in gene expression by 68% to 90% at 72 h post-injection, indicating that multi-gene dsRNA can achieve similar silencing outcomes as single-gene dsRNA. Knocking down one or all three NlCstF genes caused significant lethal phenotypes and molting disruptions. Mortality rates increased from 62.5% (dsNlCstF50) to 95.4% (dsNlCstF(50+64+77)). Additionally, silencing these genes reduced the number of eggs laid per female and hatch rates. These results highlight the critical role of NlCstF genes in the development and reproduction of N. lugens, suggesting their potential as targets for RNAi-based pest control strategies.

The brown planthopper (Nilaparvata lugens) is a major pest threatening global rice production, significantly reducing yields annually. As N. lugens increasingly develops resistance to conventional control methods, such as chemical pesticides, there is an urgent need for innovative and sustainable pest management strategies. Cleavage and Polyadenylation Specificity Factor 30 (CPSF30) is a key protein involved in mRNA 3′ end processing, yet its function in N. lugens remains poorly understood. This study aims to elucidate the role of CPSF30 in the growth and development of N. lugens and evaluate its potential as a target for RNA interference (RNAi)-based pest control strategies. We cloned and characterized the cDNA sequence of NlCPSF30, which encodes a protein of 341 amino acids containing five CCCH zinc-finger domains and two CCHC zinc-knuckle domains. Sequence alignment revealed that NlCPSF30 is highly conserved among insect species, particularly in the zinc-finger domains essential for RNA binding and processing. Phylogenetic analysis showed that NlCPSF30 is closely related to CPSF30 proteins from other hemipteran species. Expression analysis indicated that NlCPSF30 is most highly expressed in the fat body and during the adult stage, with significantly higher expression in females than in males. RNAi-mediated silencing of NlCPSF30 in third-instar nymphs resulted in severe phenotypic abnormalities, including disrupted molting and increased mortality following injection of double-stranded RNA (dsRNA) targeting NlCPSF30. Moreover, it influenced the expression of genes associated with hormone regulation, namely NlHry, NlE93, and NlKr-h1. These results suggest that NlCPSF30 is integral to critical physiological processes, with its disruption leading to increased mortality. Our findings identify NlCPSF30 as an essential gene for N. lugens’ survival and a promising target for RNAi-based pest management strategies. This study provides a valuable molecular target and theoretical insights for developing RNAi-based control methods against N. lugens.