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Review

Mechanisms of Resistance of Oryza sativa to Phytophagous Insects and Modulators Secreted by Nilaparvata lugens (Hemiptera, Delphacidae) When Feeding on Rice Plants

1
Key Laboratory of Plant Genetics and Molecular Breeding, Zhoukou Normal University, Zhoukou 466001, China
2
Henan Key Laboratory of Crop Molecular Breeding and Bioreactor, Zhoukou 466001, China
3
Henan Plant Gene and Molecular Breeding Engineering Research Center, Zhoukou 466001, China
4
Henan Crop Molecular Design Breeding and Cultivation Engineering Technology Research Center, Zhoukou 466001, China
*
Authors to whom correspondence should be addressed.
Agronomy 2025, 15(8), 1891; https://doi.org/10.3390/agronomy15081891
Submission received: 10 July 2025 / Revised: 1 August 2025 / Accepted: 4 August 2025 / Published: 6 August 2025
(This article belongs to the Special Issue New Insights into Pest and Disease Control in Rice)

Abstract

The brown planthopper, Nilaparvata lugens (Stål, 1854), is the most devastating pest of rice (Oryza sativa L.). Although insecticides are used to control this pest, host plant resistance is a more effective and economic solution. Therefore, identification of N. lugens-resistant genes and elucidation of their underlying resistance mechanisms are critical for developing elite rice cultivars with enhanced and durable resistance. Research has shown that in the long-term evolutionary arms race, rice has developed complex defense systems against N. lugens, while N. lugens has developed diverse and sophisticated strategies to overcome the plant’s defenses. This review emphasizes recent advances in the molecular interactions between rice and the N. lugens, particularly focusing on the resistance mechanisms of 17 cloned major N. lugens resistance genes, which have significantly improved our understanding of the molecular basis of rice–N. lugens interactions. We also highlight the roles of several N. lugens salivary components in activating or suppressing rice defense responses. These insights provide a foundation for developing sustainable and effective strategies to manage this devastating pest of rice.

1. Introduction

Rice (Oryza sativa L.) is a primary staple food for nearly half of the world’s population and serves as one of the most crucial food sources worldwide [1,2]. The brown planthopper, Nilaparvata lugens (Stål, 1854) (Hemiptera: Delphacidae), is one of the most destructive pests of rice [3,4]. The planthopper family Delphacidae Leach, 1815 (Hemiptera, Fulgoromorpha: Fulgoroidea) comprise 2217 species across 427 genera and six subfamilies globally [5,6]. Fossil records indicate that the oldest confirmed Delphacidae fossil is from Middle Eocene Baltic amber [5,7], with subsequent findings in Miocene deposits from Russia and Miocene fossil resins [7,8,9]. Delphacids are distributed across most terrestrial habitats worldwide, except Antarctica [10]. These insects are mainly associated with monocotyledonous plants, particularly grasses and sedges [11,12]. Some species have a wider range of host plants, feeding on horsetails and even mosses [6,13]. Economically, they are important agricultural pests, with at least 55 delphacid species feeding on 25 crops, such as rice, maize, wheat, barley, and sugarcane [6,11].
N. lugens is widely distributed across Asia, Australia, and the South Pacific islands [14]. Research has shown that N. lugens underwent a host shift from Leersia plants to rice approximately 0.25 million years ago [15,16]. Subsequently, N. lugens evolved as a monophagous insect, specializing exclusively in rice plants [17]. It is a piercing–sucking insect that directly damages rice plants by inserting its needle-like stylets into the vascular tissues to ingest phloem sap, thus indirectly affecting rice yield by acting as a vector of several disease-causing viruses, such as the rice grassy stunt virus (RGSV) and the rice ragged stunt virus (RRSV) [18,19,20,21]. N. lugens infestations have been reported to cause annual economic losses exceeding USD 300 million in rice-growing areas of Asia [22,23]. Although insecticides are used to control this pest, the extensive and long-term application of these chemicals leads to environmental risks, kills natural enemies of N. lugens, stimulates planthopper reproduction, and promotes the emergence of insecticide-resistant populations, which ultimately causes N. lugens population resurgence [23,24,25,26]. Therefore, developing novel rice varieties that exploit N. lugens resistance genes has been regarded as the most eco-friendly and low-cost approach to manage this pest [27,28,29,30].
During the evolutionary arms race between rice and its pests, N. lugens has evolved diverse adaptation strategies, including secreting saliva to overcome host defenses [31,32]. Studies have proven that, similar to other piercing–sucking herbivores, N. lugens secretes two types of saliva into plant tissues during feeding, namely the gelling saliva and the watery saliva [33,34]. The gelling saliva forms a sheath around the stylets during feeding, while the watery saliva delivers bioactive compounds, including proteins, microRNAs (miRNAs), amino acids, and fatty acids [33,35,36,37,38]. Based on their function, these bioactive compounds are categorized into elicitors and effectors [31,39,40]. Elicitors, present in insect oral secretions, trigger defense responses in plants, including increased cytoplasmic calcium levels, reactive oxygen species (ROS) bursts, MAPK activation, jasmonic acid (JA) and salicylic acid (SA) signaling pathway induction, and callose deposition [39,41]. On the other hand, effectors weaken plant defenses by interfering with immune signaling or damaging cellular structures, ultimately enabling the pest to establish successful infestations [42,43,44].
In this review, we discuss recent advances in the molecular mechanisms associated with N. lugens resistance and the roles of N. lugens elicitors and effectors in rice–N. lugens interactions. We also identify areas that require further investigation. The review will thus deepen our understanding of rice–N. lugens interactions and aid in developing sustainable and effective control measures against this economically devastating pest.

2. Genetics of N. lugens Resistance

The integration of N. lugens resistance genes into host plants has been identified as a cost-effective and eco-friendly way to manage N. lugens and promote sustainable rice production [45,46]. The diverse genetic germplasms serve as invaluable assets for developing N. lugens-resistant cultivars. To date, multiple resistance genes have been identified. Bph1, the first major N. lugens resistance gene, was identified in the indica rice variety Mudgo in 1971 [47]. Subsequently, with the development of map-based cloning and genome-wide association studies (GWAS), 46 N. lugens resistance genes were identified in cultivated varieties or wild species of rice [48,49]. Among these, 23 genes (Bph1–9, Bph17, Bph19, Bph25–26, Bph28, Bph30–33, Bph37–38, Bph42–44) were identified in the cultivated rice varieties, whereas the rest were derived from the wild species (Bph10 and Bph18 from O. australiensis; Bph1–15 from O. officinalis; Bph16, Bph20–21, and Bph23 from O. minuta; Bph22 from O. glaberrima; Bph24, Bph27, Bph29, Bph35–36, and Bph41 from O. rufipogon; Bph34, Bph39–40, and Bph45–46 from O. nivara) [27,49,50]. Rice varieties harboring single or pyramided N. lugens resistance genes have been successfully developed, promoting sustainable and eco-friendly management of N. lugens [51,52]. These findings underscore the importance of utilizing the genetic diversity of cultivated and wild species to expand the repertoire of N. lugens resistance genes, providing valuable resources for improving crop resistance via breeding. However, the enormous and diverse genetic reservoir indicates many new resistance genes likely remain to be identified.

3. Molecular Mechanisms Associated with N. lugens Resistance Genes

3.1. Classification and Structural Diversity of 17 Cloned Rice Genes Conferring Resistance to N. lugens

Researchers have successfully cloned a total of 17 N. lugens resistance-associated genes. Among these, eight genes (Bph1, Bph2, Bph7, Bph9, Bph10, Bph18, Bph21, and Bph26) have been identified as multiple alleles at the same locus, which confer varying resistance levels against different N. lugens populations [17]. Meanwhile, the remaining nine genes are located on chromosomes 3, 4, and 6 of rice [45,53,54,55,56,57,58,59]. These 17 genes can be categorized into three major types based on the amino acid domains they encode, including coiled-coil, nucleotide-binding, and leucine-rich repeat (CC-NB-LRR, CNL)-type genes; LRR-containing genes; and other types of N. lugens resistance genes (Table 1). Specifically, Bph14 encodes a CNL protein, while Bph1, Bph2, Bph7, Bph9, Bph10, Bph18, Bph21, and Bph26 encode a CC-NB-NB-LRR (CNNL) protein featuring dual NB domains [17,45]. Additionally, Bph37 encodes an atypical CNL protein lacking the LRR domain [55]. Collectively, these 10 genes are categorized as CNL-type genes. The second category comprises three N. lugens resistance genes that encode distinct LRR-containing proteins: Bph6 encodes an atypical LRR protein, whereas Bph30 and Bph40 encode proteins containing a leucine-rich repeat domain (LRD) [53,54]. The remaining four genes are classified as other types of N. lugens resistance genes. Among them, Bph15 and Bph3 encode lectin receptor-like kinases (LecRKs), bph29 encodes a B3 DNA-binding domain protein, and Bph32 encodes a protein containing a short consensus repeat (SCR) domain [56,57,58,59]. The diverse types of proteins encoded by N. lugens resistance genes indicate the high variety of N. lugens resistance mechanisms. Understanding the molecular mechanisms underlying N. lugens resistance genes will significantly enhance our comprehension of rice–N. lugens interactions.

3.2. CNL-Type Genes

CNL proteins play pivotal roles in mediating resistance against insects [61,63]. The first cloned N. lugens resistance gene was Bph14, which encodes a cytoplasm-localized CNL protein predominantly expressed in the vascular bundles of rice plants [45]. It was isolated from the highly resistant medicinal rice line B5 [64]. Initially, Du et al. found that Bph14 activates the SA signaling pathway and induces callose deposition in the phloem, thereby hindering N. lugens feeding [45]. Further investigation into the functions of BPH14’s domains revealed that the CC and NB domains of BPH14, as well as the full-length protein, form a homologous complex that interacts with OsWRKY46 and OsWRKY72 transcription factors. This interaction further enhances the accumulation and transactivation activity of OsWRKY46 and OsWRKY72 and subsequently drives the expression of the receptor-like cytoplasmic kinase gene OsRLCK281 and the callose synthase gene LOC_Os01g67364.1 by directly binding to their promoters, thus potentiating immune responses [61]. Structural studies revealed that both the domains (CC and NB) of BPH14 independently or synergistically confer N. lugens resistance comparable to the full-length protein [61]. Additionally, Guo et al. [60] found that the BPH14-interacting salivary protein (BISP) secreted by N. lugens targets the receptor-like kinase OsRLCK185 and suppresses the basal defense mechanism of susceptible rice plants. On the contrary, in resistant plants, BPH14 binds with BISP and activates host plant resistance (HPR); however, the sustained activation of HPR negatively impacts rice growth and productivity. Therefore, plants employ finely regulated mechanisms to balance immunity and growth. In rice, the fine-tuning of Bph14-mediated HPR involves the direct binding of BISP and BPH14 proteins to the autophagy receptor OsNBR1 (neighbor of BRCA1 gene 1 protein). This binding then delivers BISP to OsATG8 for degradation. OsNBR1-mediated autophagy therefore controls BISP levels. However, once feeding stops, cellular homeostasis is restored by suppressing HPR [60]. This groundbreaking study elucidated the precise mechanism underlying the interaction between BISP and the NLR receptor (Figure 1). These findings proved how NLR receptors detect insect-derived signals to activate and fine-tune host plant effector-triggered immunity (ETI). Thus, we believe that NLR proteins (such as BPH14) can be utilized as targets for developing strategies to breed crop varieties with enhanced insect resistance while maintaining balanced growth and productivity.
The Bph9 locus, encoding a rare CNNL protein with dual NB domains instead of the typical one domain, represents an allelic series on chromosome 12L; this locus includes eight N. lugens resistance genes (Bph1, Bph2, Bph7, Bph9, Bph10, Bph18, Bph21, and Bph26) [17]. Among the various proteins encoded by these genes, BPH9 confers resistance to N. lugens through the coordinated functioning of the domains (CC, NBS1, NBS2, and LRR domains) [65]. The CC domain activates a hypersensitive response (HR) specifically via the 97–115 amino acid residues, and the nucleotide-binding site 2 (NBS2) domain regulates this activation. NBS2 contains a complete set of NBS motifs that function as a molecular switch to suppress the activation of the CC domain. However, NBS1 of BPH9, due to the lack of ARC2, does not inhibit CC activity. The LRR domain of BPH9 also confers resistance to N. lugens; it functions as a signal recognizer and determines resistance specificity [65]. In short, the study proved that BPH9’s atypical dual-NBS architecture enables constitutive HR activation (via CC and regulated NBS2) coupled with LRR-mediated signal recognition, collectively conferring N. lugens resistance. Furthermore, sequence-based allelic analysis classified the Bph9 alleles into four types: Bph1/9-1 (Bph1, Bph10, Bph18, and Bph21), Bph1/9-2 (Bph2 and Bph26), Bph1/9-7 (Bph7), and Bph1/9-9 (Bph9). These allelic variants possess distinct resistance spectra; for instance, Bph1/9-1 and Bph1/9-2 demonstrate resistance against N. lugens biotypes I/III and I/II, respectively, whereas Bph1/9-7 and Bph1/9-9 exhibit broad-spectrum resistance to N. lugens biotypes I/II/III [17]. The allelic diversity of the Bph9 locus confers rice resistance to different biotypes of N. lugens, providing molecular insights into the nucleotide-binding and leucine-rich repeat (NLR)-mediated resistance mechanisms. The elucidation of this mechanism also serves as a theoretical basis for the strategic deployment of allelic variants in developing resistant rice varieties.
Bph37, which is located on the short arm of chromosome 6, is another important resistance gene that encodes an atypical CNL protein that lacks the LRR domain [55]. Research has proven that in the N. lugens-resistant rice variety SE382, this structural truncation is due to a 1 bp insertion in the second exon of the gene, which caused premature translational termination [55]. Functional complementation assays demonstrated that the expression of this cDNA in susceptible Nipponbare plants significantly enhanced N. lugens resistance in transgenic lines. In contrast, the N. lugens-susceptible rice varieties Nipponbare and Kasalath had an intact CNL protein structure [55]. The differences in the structure of this protein between varieties indicate the importance of atypical structural characteristics in N. lugens resistance. Notably, the LRR domain of resistance proteins is thought to act as a pathogen-specific receptor domain, and it also plays a role in intramolecular interactions to regulate NLR protein activity [66,67,68]. Since Bph37 lacks this canonical LRR domain, elucidating its resistance mechanism requires focused investigation into how it achieves effector recognition without LRR, as well as how its truncated structure initiates immune signaling.

3.3. LRR-Containing Genes

Another class of resistance genes encode LRR-containing proteins. Bph6 is a broad-spectrum planthopper resistance gene isolated from the cultivated rice variety Swarnalata. It is located on the long arm of chromosome 4 and encodes an exocyst-localized protein that interacts with the exocyst subunit OsEXO70E1 and promotes exocytosis [53]. BPH6 confers resistance to both N. lugens and Sogatella furcifera (Horváth, 1899) by maintaining and reinforcing the plant cell wall and thereby inhibiting stylet penetration [53]. OsEXO70H3, another member of the EXO70 paralogues, also interacts with BPH6 and regulates plant cell excretion and planthopper resistance. During this mechanism of action, OsEXO70H3 interacts with S-adenosylmethionine synthetase-like protein (SAMSL) and increases its extracellular delivery, driving lignin deposition on cell walls [62]. Wu et al. also found that the functional disruption of OsEXO70H3 and SAMSL proteins reduced the lignin content of the cell wall and thereby decreased rice resistance to planthoppers [62]. Thus, OsEXO70H3 recruits SAMSL and enhances its excretion to the apoplast, where SAMSL facilitates lignin deposition in cell walls, thereby participating in Bph6-mediated resistance. Research has also indicated that Bph6 activates cytokinin, SA, and JA signaling pathways and thereby confers broad-spectrum resistance without compromising yield [53]. These studies elucidating Bph6-mediated resistance mechanisms have indicated a crucial role for the exocyst complex and the plant cell wall. The increased thickness of cell walls in Bph6 plants allows them to act as physical barriers to hinder N. lugens stylet penetration into the plants. However, the activation mechanisms for downstream cell-wall-associated signaling partners remains unknown.
Bph30, a member of a novel family of N. lugens resistance genes, encodes a protein with two LRR domains [54]. This gene is primarily expressed in the sclerenchyma cells of the rice leaf sheath [54]. Similar to Bph6, Bph30 enhances cellulose and hemicellulose syntheses, strengthens cell walls, and thickens the sclerenchyma, thereby blocking N. lugens stylet penetration [54]. Furthermore, a study integrating transcriptomics and metabolomics indicated that Bph30-mediated resistance in rice involves the coordinated movement of primary and secondary metabolites as well as hormones through the shikimate pathway, thereby enhancing rice resistance to N. lugens [14]. Shi et al. also identified another Bph30-like gene, Bph40, in N. lugens-resistant rice varieties such as SE232, SE67, and C334 via GWAS and homology analysis [54]. Similar to Bph30, Bph40 confers resistance to N. lugens by strengthening the walls of the sclerenchyma cells. A detailed analysis revealed that the upregulation of genes associated with the cell wall and an increase in the deposition of cellulose and hemicellulose on the wall of the sclerenchyma cells are responsible for N. lugens resistance via this mechanism [54]. Furthermore, sequence homology analysis uncovered 27 Bph30-like genes in rice [54], suggesting these paralogous genes constitute a multigene family evolved for specialized defense functions, potentially serving as functional backups or regulators to fine-tune N. lugens resistance mechanisms. However, the role of these Bph30-like genes in regulating N. lugens resistance remains unexplored. Future studies should focus on deciphering their functions and leveraging their synergistic potential to enhance resistance against N. lugens.

3.4. Other Types of N. lugens Resistance Genes

Studies have identified a few other genes associated with N. lugens resistance. The Bph15 and Bph3 genes, both located on chromosome 4 and encoding lectin receptor kinases (OsLecRKs), are known to confer resistance to N. lugens [56,57]. Among the two, Bph15 confers resistance by enhancing the expression of defense-related genes, such as PR1a (basic pathogenesis-related gene 1), LOX (encoding a lipoxygenase), and CHS (encoding a peroxidase) [57]. This resistance is mediated through BPH15’s kinase domain, which interacts with actin-depolymerizing factor (ADF). Typically, ADF deficiency leads to weakened immune responses and decreased biotic stress resistance [57]. Thus, silencing of OsADF in rice consequently attenuated plant defenses against N. lugens infestation [57]. Meanwhile, Bph3, identified from the Sri Lankan rice variety Rathu Heenati, comprises a tandem cluster of three plasma membrane-localized lectin receptor kinase genes (OsLecRK1, OsLecRK2, and OsLecRK3) within a 79 kb region on the short arm of chromosome 4 [56]. Functional studies revealed that OsLecRK1, OsLecRK2, and OsLecRK3 act additively and confer broad-spectrum and durable resistance against both N. lugens and S. furcifera [56]. Among the three genes, OsLecRK1 accounts for approximately 50% of resistance, while OsLecRK2 and OsLecRK3 each contribute an additional 25% of the effect [56]. Additionally, tandem mass tag labeling combined with liquid chromatography tandem (LC-MS/MS) analysis of the Bph3 introgression line R373 revealed that Bph3 enhances rice resistance to N. lugens primarily by suppressing the downregulation of metabolic pathway-associated proteins [69]. Moreover, calcium signaling, the MAPK signaling pathway, and plant hormone signal transduction might also contribute to Bph3-mediated resistance [69]. Further biochemical characterization of OsLecRKs will reveal how these receptors perceive insect-derived signals and transduce defense responses. The recessive gene bph29, located on chromosome 6, is also known to confer resistance to N. lugens. It encodes a B3 DNA-binding protein that activates SA signaling but suppresses JA/ethylene (Et) pathways, ultimately leading to enhanced resistance against N. lugens [58]. Another gene located on chromosome 6, Bph32, encodes a plasma membrane-localized short homologous repeat sequence (SCR) protein [59]. Research has shown that Bph32 disrupts the feeding behavior and nutrient uptake pathways of N. lugens [59]. However, the components associated with Bph32-mediated resistance remain unknown.

4. N. lugens Salivary Components as Key Mediators in Rice–Insect Interactions

The devastating pest of rice, N. lugens, is a piercing–sucking insect that penetrates the tissues with specialized stylets and feeds on phloem sap [70,71,72]. During feeding, N. lugens secretes saliva containing various bioactive components, such as proteins, microRNAs (miRNAs), amino acids, and fatty acids [35,36,37,73]. These bioactive compounds play an important role in insect–plant interactions [69,74]. Recent reports on N. lugens-induced plant immunity suggest that the secreted proteins and miRNAs in saliva serve as effectors or elicitors (Figure 1 and Table 2). These findings provide novel insights into the saliva-mediated molecular mechanisms underlying plant–insect interactions and reveal promising molecular targets for the development of pest management strategies.

4.1. N. lugens Elicitors Involved in Interactions with Rice

Elicitors, which are secretory proteins found in N. lugens saliva, trigger a cascade of primary immune defense responses in the host plant rice [40,88]. Among these, salivary proteins, such as the chemosensory protein NlCSP11, trigger the SA defense pathway to modulate plant immunity. Chemosensory proteins (CSPs) are a set of proteins known to regulate insect physiology and mediate interactions with the host plant’s defense-related molecules [81]. They are small, soluble proteins predominantly localized in insect chemosensilla and secreted into plants, acting as potential effector proteins during feeding [81,89]. Overexpression of NlCSP11, a CSP of N. lugens, triggered cell death and dwarfism in N. benthamiana by activating ETI via enhanced disease susceptibility 1 (EDS1), neuregulin 1 (NRG1), and senescence-associated gene 101 (SAG101) [81]. Detailed analysis revealed that NlCSP11 induces SA-dependent systemic resistance, interacts with the recognition of CSPs (RCSP), and drives Toll-interleukin-1 receptor (TIR) domain nucleotide-binding leucine-rich repeat receptor (TNL)-mediated ETI, ultimately leading to the inhibition of NlCSP11-induced cell death and dwarfism in N. benthamiana [81]. This study demonstrated that NlCSP11, recognized by a TNL protein, promotes ETI and salicylic acid-dependent systemic resistance. These findings offer novel insights into the role of plant TNL signaling mechanisms in plant–insect interactions.
Beyond SA pathways, N. lugens elicitors can also activate plant defenses via JA signaling. For example, the Nilaparvatha lugens-secreted mucin-like protein (NlMLP), a dominant protein expressed in the salivary glands of N. lugens, serves as an elicitor once secreted into rice plants during feeding [75]. This protein is essential for salivary sheath formation during N. lugens’s penetration of rice cell walls, and its silencing disrupts N. lugens’s feeding and performance [75]. Once secreted into rice, NlMLP triggers responses, such as cell death induction, defense-related gene expression, and callose deposition [75]. These host responses are associated with Ca2+ mobilization, MEK2 MAP kinase activation, and JA signaling [75].
Oxidative burst is another defense mechanism triggered by N. lugens elicitors. Transient expression assays showed that N. lugens salivary protein 1 (NlSP1) induces diverse defense responses in Nicotiana benthamiana, such as cell death, chlorosis or dwarfism, defense-related gene upregulation, and callose deposition [76]. Studies on N. lugens secretome have identified other elicitors, such as Nl12/16/28/32/40/43, which also induce these defense responses [77]. Notably, Huang et al. found that NlSP1 also triggers hydrogen peroxide (H2O2) accumulation in N. benthamiana, suggesting its potential role in activating the oxidative burst pathway during early plant immune responses [76].
Furthermore, several N. lugens elicitors have been shown to simultaneously induce both JA signaling and H2O2 accumulation in host plants. Among these, vitellogenin (Vg) is involved in N. lugens–rice interactions, playing essential roles in insect development and fecundity [78,90]. In N. lugens, Vg is present in gelling saliva and eggs, and the N-terminal subunit of N. lugens Vg (NlVgN) functions as a key elicitor of defense responses in rice once introduced during feeding or oviposition [78]. NlVgN specifically induces cytosolic Ca2+ and H2O2 accumulation, JA and jasmonoyl-isoleucine (JA-Ile) production, and defense-related gene upregulation [78]. It also induces the emission of 11 volatile compounds, including α-pinene, sesquithujene, and α-cedrene, which attract egg parasitoids, thereby facilitating indirect defense [78]. Notably, VgN from other planthopper species also triggers these defense responses in rice [78]. The N. lugens DNAJ protein (NlDNAJB9) and NlG14 also play pivotal roles in plant–insect interactions. While NlG14 is exclusively localized to salivary glands, NlDNAJB9 exhibits significantly higher expression in salivary glands compared to other tissues, including the gut, fat body, ovaries, testes, and cuticle [79,80]. Research has shown that these proteins elicit defense responses by inducing cell death, ROS accumulation, callose deposition, and JA pathway activation in tobacco [79,80]. NlDNAJB9 also triggers Ca2+ signaling and MAPK cascades [79]. Additionally, NlDNAJB9 interacts with heat shock 70 kDa protein cognate 3 (NlHSC70-3), and NlHSC70-3 significantly represses the expression of defense-related genes NbMKK1 and NbPR1, while significantly up-regulated the expression of NbPR3 and NbPR4.. This suggests that NlHSC70-3 may modulate the plant defense response induced by NlDNAJB9, potentially through indirect mechanisms [79].

4.2. N. lugens Effectors Involved in Interactions with Rice

Insects, including herbivores, secrete effectors that suppress the defense responses of host plants [40,41,91]. One such effector is NlEG1, an endo-β-1,4-glucanase found in N. lugens salivary glands, and it facilitates stylet penetration and phloem feeding by degrading the cellulose molecules in the plant cell wall [82]. N. lugens salivary protein 7 (NlSP7) is another component of N. lugens that functions as an effector. It reduces the levels of the defensive metabolite tricin in rice and thereby promotes N. lugens feeding [92]. BISP, another effector secreted by N. lugens, binds to OsRLCK185 and suppresses rice defense responses. However, in the resistant rice cultivars, the resistance gene Bph14 specifically recognizes and degrades BISP via the autophagic pathway, triggering strong defense responses to prevent N. lugens infestation, while preserving normal plant growth and yield [60]. This study highlighted a key resistance mechanism wherein a N. lugens effector is sensed by a plant immune receptor, subsequently activating and fine-tuning Bph14-mediated HPR through autophagic regulation.
Several N. lugens effectors suppress rice defense responses by targeting the reactive oxygen species (ROS). For instance, the EF-hand calcium-binding protein (NlSEF1) suppresses rice defense responses by reducing the production of H2O2 and the accumulation of Ca2+, thereby facilitating sustained N. lugens feeding on the rice phloem [83]. Similarly, calmodulin (CaM) exhibits calcium-binding activity and suppresses H2O2 accumulation and callose deposition, promoting N. lugens penetration [84]. Another effector, heat shock 70 kDa protein cognate 3 (NIHSC70-3), suppresses flg22-induced ROS bursts and defense-related gene expression in N. benthamiana [85]. In addition, Nl14 interacts with disease resistance 1-like (OsEDR1l) and suppresses N. lugens-induced JA, JA-Ile, and H2O2 accumulation, thereby facilitating N. lugens infestation [86]. These reports indicate that effectors act by suppressing ROS to inhibit rice defense responses, thereby facilitating N. lugens infestation on rice.
N. lugens effectors also adversely affect plant hormone-related defense pathways. The odorant-binding protein NlugOBP11, the effector that is highly expressed in N. lugens salivary glands and secreted into rice tissues during feeding, is essential for N. lugens’s phloem feeding [87]. Liu et al. found that RNA interference (RNAi)-mediated silencing of NlugOBP11 decreased the total duration of salivary secretion, reduced sap sucking, and caused insect mortality, confirming that NlugOBP11 is critical for N. lugens to successfully acquire phloem nutrients [87]. Moreover, ectopic expression of NlugOBP11 in rice protoplasts and N. benthamiana leaves significantly suppressed SA biosynthesis, proving its role in suppressing plant immune responses [87]. Studies have also shown that the effector Nl14 suppresses N. lugens-induced accumulation of JA and JA-Ile in rice plants [86]. Collectively, these findings suggest that N. lugens effectors like NlugOBP11 and Nl14 disrupt plant immunity by suppressing key defense hormones, specifically SA biosynthesis and jasmonate (JA/JA-Ile) accumulation.
Recent advances in plant–insect interactions have demonstrated that N. lugens secrete salivary miRNAs as cross-kingdom effectors. One such miRNA is miR-7-5P, which is conserved across different insects and is specifically expressed in N. lugens salivary glands, with its function being to suppress rice immunity during feeding [49]. Silencing of miR-7-5P in N. lugens significantly reduced honeydew excretion, decreased phloem sap ingestion, and increased pathway duration during the feeding process, suggesting impaired N. lugens feeding performance. However, no such effects were observed on artificial diets [49]. These results indicate that miR-7-5P is essential for the feeding of N. lugens on rice plants but not on artificial diets. Moreover, the drop in feeding efficiency was rescued when N. lugens were fed on transgenic rice plants expressing miR-7-5P. This study is the first report on an miRNA functioning as an effector in N. lugens. Further studies based on target prediction and experimental testing showed that miR-7-5P targets multiple plant genes, including the immune-associated bZIP transcription factor (OsbZIP43) [49]. Consistent with this observation, the miR-7-5P-silenced insect infestation induced OsbZIP43 upregulation in rice plants. Overexpression of OsbZIP43 in tobacco conferred plant resistance against whiteflies, which was effectively suppressed by miR-7-5P [49]. These studies suggest that the conservation of miR-7-5P appears to be a newly evolved salivary effector that suppresses ‘plant immunity. N. lugens also secretes several other miRNAs, such as miR-100-5P and miR-184-3P, into rice plants to mediate the systemic regulation of host pathways [49]. The discovery of multiple miRNAs with analogous functions offers ideas for developing RNA-based pest control strategies.

5. Conclusions

In this review, we summarize recent reports on the molecular mechanisms underlying N. lugens–rice interactions and the associated components (Figure 1). Specifically, the cloning of 17 N. lugens-resistant genes and elucidation of the resistance mechanisms have laid a robust foundation for developing N. lugens-resistant rice varieties and supporting sustainable agriculture. Various components of N. lugens saliva have been identified and proven to be central mediators of N. lugens–rice interactions, including elicitors triggering defenses and effectors suppressing host immunity. These discoveries have provided novel targets for pest management.
Advances in our understanding of the N. lugens–rice interactions and the development of marker-assisted selection and gene pyramiding techniques have enabled the generation of several elite N. lugens-resistant varieties, including the pyramided lines carrying Bph14 and Bph15. However, the emergence of new N. lugens biotypes usually compromises the durability of resistance conferred by these genes. Therefore, it is imperative to identify and characterize new resistance genes from diverse genetic resources, such as wild species, and deciphering the precise defense mechanism. This effort will further help in generating cultivars with durable, broad-spectrum resistance, especially against new N. lugens biotypes. Additionally, while substantial research has elucidated the mechanisms of N. lugens resistance genes, the specific N. lugens effectors that interact with resistance genes—along with their underlying molecular mechanisms—remain largely uncharacterized, with the exception of Bph14. Thus, future efforts should be given to systematic investigation into these effector–resistance gene interaction networks and molecular mechanisms, to lay a theoretical foundation for developing durable resistance strategies against N. lugens.
Although advances in genomic, transcriptomic, and proteomic technologies have accelerated the identification and characterization of elicitors and effectors mediating N. lugens–rice interactions, only a limited number of their corresponding host targets have been identified. Subsequent clarification of defense pathways and molecular mechanisms will deepen our understanding of rice resistance to N. lugens and, critically, may enable the design of novel pest control strategies.
Thus, our review establishes that the introduction of resistance genes into rice cultivars is the most effective and eco-friendly strategy for managing N. lugens populations. Further characterizing N. lugens resistance genes and elucidating the molecular mechanisms underlying N. lugens–rice interactions will be crucial for developing novel varieties with durable, broad-spectrum resistance against the evolving pest biotypes.

Author Contributions

Conceptualization, K.X. and X.S.; writing—original draft, X.Z., W.W. and Y.H.; writing—review and editing, X.Z. and X.S.; visualization, X.Z., W.W. and Y.H.; supervision, K.X. and X.S.; funding acquisition, K.X. and X.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Department of Science and Technology Planning Project of Henan Province (grant numbers 242102110299 and 252102110322).

Acknowledgments

We thank Hongfei Shang (Zhoukou Normal University) for the help in creating and optimizing the Figure 1.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Abd El-Aty, M.S.; Abo-Youssef, M.I.; Galal, A.A.; Salama, A.M.; Salama, A.A.; El-Shehawi, A.M.; Elseehy, M.M.; El-Saadony, M.T.; El-Tahan, A.M. Genetic behavior of earliness and yield traits of some rice (Oryza sativa L.) genotypes. Saudi J. Biol. Sci. 2022, 29, 2691–2697. [Google Scholar] [CrossRef] [PubMed]
  2. Yele, Y.; Chander, S.; Suroshe, S.S.; Nebapure, S.; Tenguri, P.; Pattathanam Sundaran, A. Ecological engineering in low land rice for brown plant hopper, Nilaparvata lugens (Stål) management. PeerJ 2023, 11, e15531. [Google Scholar] [CrossRef] [PubMed]
  3. Liu, F.; Li, X.; Zhao, M.; Guo, M.; Han, K.; Dong, X.; Zhao, J.; Cai, W.; Zhang, Q.; Hua, H. Ultrabithorax is a key regulator for the dimorphism of wings, a main cause for the outbreak of planthoppers in rice. Natl. Sci. Rev. 2020, 7, 1181–1189. [Google Scholar] [CrossRef] [PubMed]
  4. Hu, Q.L.; Zhuo, J.C.; Fang, G.Q.; Lu, J.B.; Ye, Y.X.; Li, D.T.; Lou, Y.H.; Zhang, X.Y.; Chen, X.; Wang, S.L.; et al. The genomic history and global migration of a windborne pest. Sci. Adv. 2024, 10, eadk3852. [Google Scholar] [CrossRef]
  5. Urban, J.M.; Cryan, J.R. Evolution of the planthoppers (insecta: Hemiptera: Fulgoroidea). Mol. Phylogenetics Evol. 2007, 42, 556–572. [Google Scholar] [CrossRef]
  6. Markevich, D.; Walczak, M.; Borodin, O.; Szwedo, J.; Brożek, J. Morphological reassessment of the movable calcar of delphacid planthoppers (hemiptera: Fulgoromorpha: Delphacidae). Sci. Rep. 2021, 11, 22294. [Google Scholar] [CrossRef]
  7. Gębicki, C.; Szwedo, J. The first ugyopine planthopper Serafinana perperunae gen. and sp. n. from eocene baltic amber (hemiptera, fulgoroidea: Delphacidae). Pol.J. Entomol./Pol. Pismo Entomol. 2000, 69, 389–395. [Google Scholar]
  8. Szwedo, J.; Bourgoin, T.; Lefèbvre, F. Fossil Planthoppers (Hemiptera Fulgoromorpha) of the World. An Annotated Catalogue with Notes on Hemiptera Classification; Studio 1: Warszawa, Poland, 2004; 199p. [Google Scholar]
  9. Solórzano Kraemer, M.M. Systematic, palaeoecology, and palaeobiogeography of the insect fauna from mexican amber. Palaeontogr. Abt. A 2007, 282, 1–133. [Google Scholar] [CrossRef]
  10. Urban, J.M.; Bartlett, C.R.; Cryan, J.R. Evolution of delphacidae (hemiptera: Fulgoroidea): Combined-evidence phylogenetics reveals importance of grass host shifts. Syst. Entomol. 2010, 35, 678–691. [Google Scholar] [CrossRef]
  11. Huang, Y.X.; Zheng, L.F.; Bartlett, C.R.; Qin, D.Z. Resolving phylogenetic relationships of delphacini and tropidocephalini (hemiptera: Delphacidae: Delphacinae) as inferred from four genetic loci. Sci. Rep. 2017, 7, 3319. [Google Scholar] [CrossRef]
  12. Wilson, S.W.; Mitter, C.; Denno, R.F.; Wilson, M.R. Evolutionary patterns of host plant use by delphacid planthoppers and their relatives. In Planthoppers: Their Ecology and Management; Denno, R.F., Perfect, T.J., Eds.; Chapman & Hall: Boca Raton, FL, USA, 1994; pp. 7–113. [Google Scholar]
  13. Wheeler, A. Bryophagy in the auchenorrhyncha: Seasonal history and habits of a moss specialist, javesella opaca (beamer) (fulgoroidea: Delphacidae). Proc. Entomol. Soc. Wash. 2003, 105, 599–610. [Google Scholar]
  14. Shi, S.; Zha, W.; Yu, X.; Wu, Y.; Li, S.; Xu, H.; Li, P.; Li, C.; Liu, K.; Chen, J.; et al. Integrated transcriptomics and metabolomics analysis provide insight into the resistance response of rice against brown planthopper. Front. Plant Sci. 2023, 14, 1213257. [Google Scholar] [CrossRef] [PubMed]
  15. Kumar, S.; Singh, H. Studies on the influence of insecticides and bio-pesticides for the management of Brown plant hopper, Nilaparvata lugens (Stal) in the condition of western up (India). Front. Plant Sci. 2021, 41, 1441–1449. [Google Scholar] [CrossRef]
  16. Jones, P.; Gacesa, P.; Butlin, R. Systematics of brown planthopper and related species using nuclear. Ecol. Agric. Pests Biochem. Approaches 1996, 53, 133. [Google Scholar]
  17. Zhao, Y.; Huang, J.; Wang, Z.; Jing, S.; Wang, Y.; Ouyang, Y.; Cai, B.; Xin, X.-F.; Liu, X.; Zhang, C.; et al. Allelic diversity in an NLR geneBPH9enables rice to combat planthopper variation. Proc. Natl. Acad. Sci. USA 2016, 113, 12850–12855. [Google Scholar] [CrossRef]
  18. Yan, L.; Luo, T.; Huang, D.; Wei, M.; Ma, Z.; Liu, C.; Qin, Y.; Zhou, X.; Lu, Y.; Li, R.; et al. Recent advances in molecular mechanism and breeding utilization of brown planthopper resistance genes in rice: An integrated review. Int. J. Mol. Sci. 2023, 24, 12061. [Google Scholar] [CrossRef] [PubMed]
  19. Ye, Y.; Xiong, S.; Guan, X.; Tang, T.; Zhu, Z.; Zhu, X.; Hu, J.; Wu, J.; Zhang, S. Insight into rice resistance to the brown planthopper: Gene cloning, functional analysis, and breeding applications. Int. J. Mol. Sci. 2024, 25, 13397. [Google Scholar] [CrossRef] [PubMed]
  20. Mishra, A.; Barik, S.R.; Pandit, E.; Yadav, S.S.; Das, S.R.; Pradhan, S.K. Genetics, mechanisms anddeployment of brown planthopper resistance genes in rice. Crit. Rev. Plant Sci. 2022, 41, 91–127. [Google Scholar] [CrossRef]
  21. Li, C.; Xiong, Z.; Fang, C.; Liu, K. Transcriptome and metabolome analyses reveal the responses of brown planthoppers to RH resistant rice cultivar. Front. Physiol. 2022, 13, 1018470. [Google Scholar] [CrossRef]
  22. Zhu, L.; Li, H.; Tao, Z.; Ma, F.; Wu, S.; Miao, X.; Cao, L.; Shi, Z. The microRNA OsmiR393 regulates rice brown planthopper resistance by modulating the auxin-ROS signaling cross-talk. Sci. Adv. 2025, 11, eadu6722. [Google Scholar] [CrossRef]
  23. Khan, M.; Han, C.; Choi, N.; Kim, J. RNAseq-based carboxylesterase Nl-EST1 gene expression plasticity identification and its potential involvement in fenobucarb resistance in the brown planthopper Nilaparvata lugens. Insects 2024, 15, 743. [Google Scholar] [CrossRef] [PubMed]
  24. Wu, J.; Ge, L.; Liu, F.; Song, Q.; Stanley, D. Pesticide-induced planthopper population resurgence in rice cropping systems. Annu. Rev. Entomol. 2020, 65, 409–429. [Google Scholar] [CrossRef] [PubMed]
  25. Yang, H.H.; Wang, Y.X.; Xiao, J.; Jia, Y.F.; Liu, F.; Wang, W.X.; Wei, Q.; Lai, F.X.; Fu, Q.; Wan, P.-J. Defense regulatory network associated with circRNA in rice in response to brown planthopper infestation. Plants 2024, 13, 373. [Google Scholar] [CrossRef] [PubMed]
  26. Wang, X.; Guo, X.; Ma, X.; Luo, L.; Fang, Y.; Zhao, N.; Han, Y.; Wei, Z.; Liu, F.; Qin, B.; et al. Development of new rice (Oryza. sativa L.) breeding lines through marker-assisted introgression and pyramiding of brown planthopper, blast, bacterial leaf blight resistance, and aroma genes. Agronomy 2021, 11, 2525. [Google Scholar] [CrossRef]
  27. Sriram, M.; Manonmani, S.; Gopalakrishnan, C.; Sheela, V.; Shanmugam, A.; Revanna Swamy, K.M.; Suresh, R. Breeding for brown plant hopper resistance in rice: Recent updates and future perspectives. Mol. Biol. Rep. 2024, 51, 1038. [Google Scholar] [CrossRef]
  28. Jiang, H.; Hu, J.; Li, Z.; Liu, J.; Gao, G.; Zhang, Q.; Xiao, J.; He, Y. Evaluation and breeding application of six brown planthopper resistance genes in rice maintainer line Jin 23B. Rice 2018, 11, 22. [Google Scholar] [CrossRef]
  29. Balachiranjeevi, C.H.; Prahalada, G.D.; Mahender, A.; Jamaloddin, M.; Sevilla, M.A.L.; Marfori-Nazarea, C.M.; Vinarao, R.; Sushanto, U.; Baehaki, S.E.; Li, Z.K.; et al. Identification of a novel locus, BPH38(t), conferring resistance to brown planthopper (Nilaparvata lugens Stal.) using early backcross population in rice (Oryza sativa L.). Euphytica 2019, 215, 185. [Google Scholar] [CrossRef]
  30. Sani Haliru, B.; Rafii, M.Y.; Mazlan, N.; Ramlee, S.I.; Muhammad, I.; Silas Akos, I.; Halidu, J.; Swaray, S.; Rini Bashir, Y. Recent strategies for detection and improvement of brown planthopper resistance genes in rice: A Review. Plants 2020, 9, 1202. [Google Scholar] [CrossRef]
  31. Prajapati, V.K.; Vijayan, V.; Vadassery, J. Secret weapon of insects: The oral secretion cocktail and its modulation of host immunity. Plant Cell Physiol. 2024, 65, 1213–1223. [Google Scholar] [CrossRef]
  32. Mou, D.F.; Kundu, P.; Pingault, L.; Puri, H.; Shinde, S.; Louis, J. Monocot crop–aphid interactions: Plant resilience and aphid adaptation. Curr. Opin. Insect Sci. 2023, 57, 101038. [Google Scholar] [CrossRef]
  33. Huang, H.J.; Wang, Y.Z.; Li, L.L.; Lu, H.B.; Lu, J.B.; Wang, X.; Ye, Z.X.; Zhang, Z.L.; He, Y.J.; Lu, G.; et al. Planthopper salivary sheath protein LsSP1 contributes to manipulation of rice plant defenses. Nat. Commun. 2023, 14, 737. [Google Scholar] [CrossRef]
  34. Huang, H.J.; Zhang, C.X.; Hong, X.Y. How does saliva function in planthopper–host interactions? Arch. Insect Biochem. 2019, 100, e21537. [Google Scholar] [CrossRef]
  35. Zhang, Z.L.; Wang, X.J.; Lu, J.B.; Lu, H.B.; Ye, Z.X.; Xu, Z.T.; Zhang, C.; Chen, J.P.; Li, J.M.; Zhang, C.X.; et al. Cross-kingdom RNA interference mediated by insect salivary microRNAs may suppress plant immunity. Proc. Natl. Acad. Sci. USA 2024, 121, e2318783121. [Google Scholar] [CrossRef] [PubMed]
  36. Kallure, G.S.; Kumari, A.; Shinde, B.A.; Giri, A.P. Characterized constituents of insect herbivore oral secretions and their influence on the regulation of plant defenses. Phytochemistry 2022, 193, 113008. [Google Scholar] [CrossRef]
  37. Han, W.H.; Ji, S.X.; Zhang, F.B.; Song, H.D.; Wang, J.X.; Fan, X.P.; Xie, R.; Liu, S.S.; Wang, X.W. A small RNA effector conserved in herbivore insects suppresses host plant defense by cross-kingdom gene silencing. Mol. Plant 2025, 18, 437–456. [Google Scholar] [CrossRef]
  38. Mahanta, D.K.; Komal, J.; Samal, I.; Bhoi, T.K.; Kumar, P.V.D.; Mohapatra, S.; Athulya, R.; Majhi, P.K.; Mastinu, A. Plant defense responses to insect herbivores through molecular signaling, secondary metabolites, and associated epigenetic regulation. Plant Environ. Interact. 2025, 6, e70035. [Google Scholar] [CrossRef]
  39. Ma, X.; Yin, Z.; Li, H.; Guo, J. Roles of herbivorous insects salivary proteins. Heliyon 2024, 10, e29201. [Google Scholar] [CrossRef]
  40. Snoeck, S.; Guayazán-Palacios, N.; Steinbrenner, A.D. Molecular tug-of-war: Plant immune recognition of herbivory. Plant Cell 2022, 34, 1497–1513. [Google Scholar] [CrossRef] [PubMed]
  41. Wang, H.; Shi, S.; Hua, W. Advances of herbivore-secreted elicitors and effectors in plant-insect interactions. Front. Plant Sci. 2023, 14, 1176048. [Google Scholar] [CrossRef] [PubMed]
  42. Ji, R.; Fu, J.; Shi, Y.; Li, J.; Jing, M.; Wang, L.; Yang, S.; Tian, T.; Wang, L.; Ju, J.; et al. Vitellogenin from planthopper oral secretion acts as a novel effector to impair plant defenses. New Phytol. 2021, 232, 802–817. [Google Scholar] [CrossRef]
  43. Rodriguez, P.A.; Escudero-Martinez, C.; Bos, J.I.B. An aphid effector targets trafficking protein VPS52 in a host-specific manner to promote virulence. Plant Physiol. 2017, 173, 1892–1903. [Google Scholar] [CrossRef]
  44. Hancock, R.; Xia, A.; Dou, D.; Wu, Y.; Wu, S.; Zuo, K.; Xia, Q.; Nyawira, K.T.; Liang, D.; Zhang, M.; et al. The mirid bug apolygus lucorum deploys a glutathione peroxidase as a candidate effector to enhance plant susceptibility. J. Exp. Bot. 2020, 71, 2701–2712. [Google Scholar] [CrossRef]
  45. Du, B.; Zhang, W.; Liu, B.; Hu, J.; Wei, Z.; Shi, Z.; He, R.; Zhu, L.; Chen, R.; Han, B.; et al. Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc. Natl. Acad. Sci. USA 2009, 106, 22163–22168. [Google Scholar] [CrossRef]
  46. Shar, S.B.D.; Nguyen, C.D.; Sanada-Morimura, S.; Yasui, H.; Zheng, S.H.; Fujita, D. Development and characterization of near-isogenic lines for brown planthopper resistance genes in the genetic background of japonica rice ‘Sagabiyori’. Breed. Sci. 2023, 73, 382–392. [Google Scholar] [CrossRef] [PubMed]
  47. Hirabayashi, H.; Ogawa, T. PFLP mapping of Bph-1 (brown planthopper resistance gene) in rice. Breed. Sci. 1995, 45, 369–371. [Google Scholar]
  48. Kaur, P.; Neelam, K.; Sarao, P.S.; Saini, N.S.; Dhir, Y.W.; Khanna, R.; Vikal, Y.; Singh, K. Mapping of a novel recessive brown planthopper resistance gene bph46 from wild rice (Oryza nivara). Euphytica 2024, 220, 61. [Google Scholar] [CrossRef]
  49. Zhang, X.; Gu, D.; Liu, D.; Hassan, M.A.; Yu, C.; Wu, X.; Huang, S.; Bian, S.; Wei, P.; Li, J. Recent advances in gene mining and hormonal mechanism for brown planthopper resistance in rice. Int. J. Mol. Sci. 2024, 25, 12965. [Google Scholar] [CrossRef]
  50. Ishwarya, L.V.G.; Vanisri, S.; Basavaraj, P.S.; Sreedhar, M.; Jhansi, L.V.; Muntazir, M.; Gireesh, C.; Pushpavalli, S.N.C.V.L. Harnessing advanced genomic approaches to unveil and enhance brown planthopper resistance in rice. Rice Sci. 2025, 32, 339–352. [Google Scholar] [CrossRef]
  51. Muduli, L.; Pradhan, S.K.; Mishra, A.; Bastia, D.N.; Samal, K.C.; Agrawal, P.K.; Dash, M. Understanding brown planthopper resistance in rice: Genetics, biochemical and molecular breeding approaches. Rice Sci. 2021, 28, 532–546. [Google Scholar] [CrossRef]
  52. Kamal, M.M.; Nguyen, C.D.; Sanada-Morimura, S.; Zheng, S.-H.; Fujita, D. Development of pyramided lines carrying brown planthopper resistance genes in the genetic background of Indica Group rice (Oryza sativa L.) variety ‘IR64’. Breed. Sci. 2023, 73, 450–456. [Google Scholar] [CrossRef]
  53. Guo, J.; Xu, C.; Wu, D.; Zhao, Y.; Qiu, Y.; Wang, X.; Ouyang, Y.; Cai, B.; Liu, X.; Jing, S.; et al. Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat. Genet. 2018, 50, 297–306. [Google Scholar] [CrossRef] [PubMed]
  54. Shi, S.; Wang, H.; Nie, L.; Tan, D.; Zhou, C.; Zhang, Q.; Li, Y.; Du, B.; Guo, J.; Huang, J.; et al. Bph30 confers resistance to brown planthopper by fortifying sclerenchyma in rice leaf sheaths. Mol. Plant 2021, 14, 1714–1732. [Google Scholar] [CrossRef]
  55. Zhou, C.; Zhang, Q.; Chen, Y.; Huang, J.; Guo, Q.; Li, Y.; Wang, W.; Qiu, Y.; Guan, W.; Zhang, J.; et al. Balancing selection and wild gene pool contribute to resistance in global rice germplasm against planthopper. J. Integr. Plant Biol. 2021, 63, 1695–1711. [Google Scholar] [CrossRef]
  56. Liu, Y.; Wu, H.; Chen, H.; Liu, Y.; He, J.; Kang, H.; Sun, Z.; Pan, G.; Wang, Q.; Hu, J.; et al. A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nat. Biotechnol. 2014, 33, 301–305. [Google Scholar] [CrossRef]
  57. Cheng, X.; Wu, Y.; Guo, J.; Du, B.; Chen, R.; Zhu, L.; He, G. A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J. 2013, 76, 687–698. [Google Scholar] [CrossRef]
  58. Wang, Y.; Cao, L.; Zhang, Y.; Cao, C.; Liu, F.; Huang, F.; Qiu, Y.; Li, R.; Lou, X. Map-based cloning and characterization of BPH29, a B3 domain-containing recessive gene conferring brown planthopper resistance in rice. J. Exp. Bot. 2015, 66, 6035–6045. [Google Scholar] [CrossRef]
  59. Ren, J.; Gao, F.; Wu, X.; Lu, X.; Zeng, L.; Lv, J.; Su, X.; Luo, H.; Ren, G. Bph32, a novel gene encoding an unknown SCR domain-containing protein, confers resistance against the brown planthopper in rice. Sci. Rep. 2016, 6, 37645. [Google Scholar] [CrossRef]
  60. Guo, J.; Wang, H.; Guan, W.; Guo, Q.; Wang, J.; Yang, J.; Peng, Y.; Shan, J.; Gao, M.; Shi, S.; et al. A tripartite rheostat controls self-regulated host plant resistance to insects. Nature 2023, 618, 799–807. [Google Scholar] [CrossRef]
  61. Hu, L.; Wu, Y.; Wu, D.; Rao, W.; Guo, J.; Ma, Y.; Wang, Z.; Shangguan, X.; Wang, H.; Xu, C.; et al. The coiled-coil and nucleotide binding domains of Brown Planthopper Resistance14 function in signaling and resistance against planthopper in rice. Plant Cell 2017, 29, 3157–3185. [Google Scholar] [CrossRef] [PubMed]
  62. Wu, D.; Guo, J.; Zhang, Q.; Shi, S.; Guan, W.; Zhou, C.; Chen, R.; Du, B.; Zhu, L.; He, G. Necessity of rice resistance to planthoppers for OsEXO70H3 regulating SAMSL excretion and lignin deposition in cell walls. New Phytol. 2022, 234, 1031–1046. [Google Scholar] [CrossRef] [PubMed]
  63. Zhong, Y.; Zhang, X.; Shi, Q.; Cheng, Z.-M. Adaptive evolution driving the young duplications in six rosaceae species. BMC Genom. 2021, 22, 112. [Google Scholar] [CrossRef]
  64. Huang, Z.; He, G.; Shu, L.; Li, X.; Zhang, Q. Identification and mapping of two brown planthopper resistance genes in rice. Theor. Appl. Genet. 2001, 102, 929–934. [Google Scholar] [CrossRef]
  65. Wang, Z.; Huang, J.; Nie, L.; Hu, Y.; Zhang, N.; Guo, Q.; Guo, J.; Du, B.; Zhu, L.; He, G.; et al. Molecular and functional analysis of a brown planthopper resistance protein with two nucleotide-binding site domains. J. Exp. Bot. 2021, 72, 2657–2671. [Google Scholar] [CrossRef]
  66. Slootweg, E.J.; Spiridon, L.N.; Roosien, J.; Butterbach, P.; Pomp, R.; Westerhof, L.; Wilbers, R.; Bakker, E.; Bakker, J.; Petrescu, A.-J. Structural determinants at the interface of the ARC2 and leucine-rich repeat domains control the activation of the plant immune receptors Rx1 and Gpa2. Plant Physiol. 2013, 162, 1510–1528. [Google Scholar] [CrossRef] [PubMed]
  67. Takken, F.L.; Goverse, A. How to build a pathogen detector: Structural basis of NB-LRR function. Curr. Opin. Plant Biol. 2012, 15, 375–384. [Google Scholar] [CrossRef]
  68. Zipfel, C. Plant pattern-recognition receptors. Trends Immunol. 2014, 35, 345–351. [Google Scholar] [CrossRef] [PubMed]
  69. Qing, D.; Chen, W.; Li, J.; Lu, B.; Huang, S.; Chen, L.; Zhou, W.; Pan, Y.; Huang, J.; Wu, H.; et al. TMT-based quantitative proteomics analysis of defense responses induced by the Bph3 gene following brown planthopper infection in rice. BMC Plant Biol. 2024, 24, 1092. [Google Scholar] [CrossRef]
  70. Li, Y.; Cheah, B.H.; Fang, Y.-F.; Kuang, Y.-H.; Lin, S.-C.; Liao, C.-T.; Huang, S.-H.; Lin, Y.-F.; Chuang, W.-P. Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores. BMC Plant Biol. 2021, 21, 306. [Google Scholar] [CrossRef] [PubMed]
  71. Shen, W.; Zhang, X.; Liu, J.; Tao, K.; Li, C.; Xiao, S.; Zhang, W.; Li, J.F. Plant elicitor peptide signalling confers rice resistance to piercing-sucking insect herbivores and pathogens. Plant Biotechnol. J. 2022, 20, 991–1005. [Google Scholar] [CrossRef]
  72. Qi, L.; Li, J.; Li, S.; Li, J.; Wang, H.; Yang, L.; Tan, X.; Zhao, Z.; Luo, G.; Jing, M.; et al. An insect salivary sheath protein triggers plant resistance to insects and pathogens as a conserved HAMP. Adv. Sci. 2025, 12, e2415474. [Google Scholar] [CrossRef]
  73. Jiang, Y.; Zhang, X.Y.; Li, S.; Xie, Y.C.; Luo, X.M.; Yang, Y.; Pu, Z.; Zhang, L.; Lu, J.B.; Huang, H.J.; et al. Rapid intracellular acidification is a plant defense response countered by the brown planthopper. Curr. Biol. 2024, 34, 5017–5027. [Google Scholar] [CrossRef]
  74. Ray, S.; Gaffor, I.; Acevedo, F.E.; Helms, A.; Chuang, W.P.; Tooker, J.; Felton, G.W.; Luthe, D.S. Maize plants recognize herbivore-associated cues from caterpillar frass. J. Chem. Ecol. 2015, 41, 781–792. [Google Scholar] [CrossRef]
  75. Shangguan, X.; Zhang, J.; Liu, B.; Zhao, Y.; Wang, H.; Wang, Z.; Guo, J.; Rao, W.; Jing, S.; Guan, W.; et al. A mucin-like protein of planthopper is required for feeding and induces immunity response in plants. Plant Physiol. 2018, 176, 552–565. [Google Scholar] [CrossRef]
  76. Huang, J.; Zhang, N.; Shan, J.; Peng, Y.; Guo, J.; Zhou, C.; Shi, S.; Zheng, X.; Wu, D.; Guan, W.; et al. Salivary protein 1 of brown planthopper is required for survival and induces immunity response in plants. Front. Plant Sci. 2020, 11, 571280. [Google Scholar] [CrossRef] [PubMed]
  77. Rao, W.; Zheng, X.; Liu, B.; Guo, Q.; Guo, J.; Wu, Y.; Shangguan, X.; Wang, H.; Wu, D.; Wang, Z.; et al. Secretome analysis and in planta expression of salivary proteins identify candidate effectors from the brown planthopper Nilaparvata lugens. Mol. Plant Microbe In 2019, 32, 227–239. [Google Scholar] [CrossRef] [PubMed]
  78. Zeng, J.; Ye, W.; Hu, W.; Jin, X.; Kuai, P.; Xiao, W.; Jian, Y.; Turlings, T.C.J.; Lou, Y. The N-terminal subunit of vitellogenin in planthopper eggs and saliva acts as a reliable elicitor that induces defenses in rice. New Phytol. 2023, 238, 1230–1244. [Google Scholar] [CrossRef]
  79. Gao, H.; Lin, X.; Yuan, X.; Zou, J.; Zhang, H.; Zhang, Y.; Liu, Z.; Hancock, R. The salivary chaperone protein NlDNAJB9 of Nilaparvata lugens activates plant immune responses. J. Exp. Bot. 2023, 74, 6874–6888. [Google Scholar] [CrossRef] [PubMed]
  80. Gao, H.; Zou, J.; Lin, X.; Zhang, H.; Yu, N.; Liu, Z.; Foyer, C. Nilaparvata lugens salivary protein NlG14 triggers defense response in plants. J. Exp. Bot. 2022, 73, 7477–7487. [Google Scholar] [CrossRef] [PubMed]
  81. Rao, W.; Ma, T.; Cao, J.; Zhang, Y.; Chen, S.; Lin, S.; Liu, X.; He, G.; Wan, L. Recognition of a salivary effector by the TNL protein RCSP promotes effector-triggered immunity and systemic resistance in Nicotiana benthamiana. J. Integr. Plant Biol. 2024, 67, 150–168. [Google Scholar] [CrossRef]
  82. Ji, R.; Ye, W.; Chen, H.; Zeng, J.; Li, H.; Yu, H.; Li, J.; Lou, Y. A salivary endo-β-1,4-glucanase acts as an effector that enables the brown planthopper to feed on rice. Plant Physiol. 2017, 173, 1920–1932. [Google Scholar] [CrossRef]
  83. Ye, W.; Yu, H.; Jian, Y.; Zeng, J.; Ji, R.; Chen, H.; Lou, Y. A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice. Sci. Rep. 2017, 7, 40498. [Google Scholar] [CrossRef]
  84. Fu, J.; Shi, Y.; Wang, L.; Tian, T.; Li, J.; Gong, L.; Zheng, Z.; Jing, M.; Fang, J.; Ji, R. Planthopper-secreted salivary calmodulin acts as an effector for defense responses in rice. Front. Plant Sci. 2022, 13, 841378. [Google Scholar] [CrossRef] [PubMed]
  85. Yang, H.; Zhang, X.; Li, H.; Ye, Y.; Li, Z.; Han, X.; Hu, Y.; Zhang, C.; Jiang, Y. Heat shock 70 kDa protein cognate 3 of brown planthopper is required for survival and suppresses immune response in plants. Insects 2022, 13, 299. [Google Scholar] [CrossRef]
  86. Fu, J.; Li, S.; Li, j.; Zhao, Z.; Li, J.; Tan, X.; Yu, S.; Jing, M.; Zhu-Salzman, K.; Fang, J.; et al. An insect effector mimics its host immune regulator to undermine plant immunity. Adv. Sci. 2025, 12, e2409186. [Google Scholar] [CrossRef]
  87. Liu, H.; Wang, C.; Qiu, C.-L.; Shi, J.-H.; Sun, Z.; Hu, X.-J.; Liu, L.; Wang, M.-Q. A salivary odorant-binding protein mediates Nilaparvata lugens feeding and host plant phytohormone suppression. Int. J. Mol. Sci. 2021, 22, 4988. [Google Scholar] [CrossRef]
  88. Filippi, A.; Petrussa, E.; Boscutti, F.; Vuerich, M.; Vrhovsek, U.; Rabiei, Z.; Braidot, E. Bioactive polyphenols modulate enzymes Involved in grapevine pathogenesis and chitinase activity at increasing complexity levels. Int. J. Mol. Sci. 2019, 20, 6357. [Google Scholar] [CrossRef]
  89. Zhang, Y.; Fu, Y.; Liu, X.; Francis, F.; Fan, J.; Liu, H.; Wang, Q.; Sun, Y.; Zhang, Y.; Chen, J. SmCSP4 from aphid saliva stimulates salicylic acid-mediated defence responses in wheat by interacting with transcription factor TaWKRY76. Plant Biotechnol. J. 2023, 21, 2389–2407. [Google Scholar] [CrossRef]
  90. Shen, Y.; Chen, Y.Z.; Lou, Y.; Zhang, C. Vitellogenin and vitellogenin-like genes in the brown planthopper. Front. Physiol. 2019, 10, 1181. [Google Scholar] [CrossRef]
  91. Su, Q.; Yang, F.; Hu, Y.; Peng, Z.; Huang, T.; Tong, H.; Zhang, R.; Yang, Y.; Zhou, Z.; Liang, P.; et al. Flavonoids enhance tomato plant resistance to whitefly by interfering with the expression of a salivary effector. Plant Physiol. 2025, 197, kiaf101. [Google Scholar] [CrossRef] [PubMed]
  92. Gong, G.; Yuan, L.Y.; Li, Y.F.; Xiao, H.X.; Li, Y.F.; Zhang, Y.; Wu, W.J.; Zhang, Z.F. Salivary protein 7 of the brown planthopper functions as an effector for mediating tricin metabolism in rice plants. Sci. Rep. 2022, 12, 3205. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Model of rice–N. lugens interactions. During feeding, the N. lugens secrete elicitors and effectors into rice cells. Elicitors activate a complex series of plant defenses, such as cytosolic Ca2+ accumulation, ROS burst, and the upregulation of JA and SA. However, N. lugens secrete effectors to suppress these defense responses. The N. lugens resistance genes in rice encode different types of immunity receptors that recognize effectors, triggering effector-triggered immunity. This immune response involves the modulation of phytohormone signaling pathways and reinforcement of the leaf sheath cell walls, ultimately preventing N. lugens from successfully sucking phloem sap. ROS, reactive oxygen species; SA, salicylic acid; JA, jasmonic acid; ?, uncharacterized salivary components of N. lugens or unidentified rice target proteins of known salivary proteins during rice–N. lugens interactions.
Figure 1. Model of rice–N. lugens interactions. During feeding, the N. lugens secrete elicitors and effectors into rice cells. Elicitors activate a complex series of plant defenses, such as cytosolic Ca2+ accumulation, ROS burst, and the upregulation of JA and SA. However, N. lugens secrete effectors to suppress these defense responses. The N. lugens resistance genes in rice encode different types of immunity receptors that recognize effectors, triggering effector-triggered immunity. This immune response involves the modulation of phytohormone signaling pathways and reinforcement of the leaf sheath cell walls, ultimately preventing N. lugens from successfully sucking phloem sap. ROS, reactive oxygen species; SA, salicylic acid; JA, jasmonic acid; ?, uncharacterized salivary components of N. lugens or unidentified rice target proteins of known salivary proteins during rice–N. lugens interactions.
Agronomy 15 01891 g001
Table 1. Plant defense mechanisms of N. lugens resistance genes.
Table 1. Plant defense mechanisms of N. lugens resistance genes.
GeneEncoded ProteinDefense MechanismRef.
Bph14CC-NB-LRRActivate SA, induce callose deposition[45]
Bind with BISP and activate NBR1-mediated autophagy[60]
Interact with OsWRKY46 and OsWRKY72 and enhance their transactivation activity[61]
Bph9CC-NB-NB-LRRActivate SA[17]
Bph1CC-NB-NB-LRR-[17]
Bph2CC-NB-NB-LRR-[17]
Bph7CC-NB-NB-LRR-[17]
Bph10CC-NB-NB-LRR-[17]
Bph18CC-NB-NB-LRR-[17]
Bph21CC-NB-NB-LRR-[17]
Bph26CC-NB-NB-LRR-[17]
Bph37CC-NB-[55]
Bph6Atypical LRRInteract with OsEXO70E1 and promote exocytosis; reinforce plant cell wall; activate SA, JA, and CK[53]
Interact with OsEXO70H3, which recruit SAMSL to enhance lignin deposition in cell wall[62]
Bph30LRDEnhance the synthesis of cellulose and hemicellulose in cell wall[54]
Bph40LRDEnhance cell wall[54]
Bph15LRKInteract with OsADF; enhance the expression of OsPR1a, OsLOX, and
OsCHS
[57]
Bph3LRK-[56]
Bph29B3 DNA-bindingActivate SA, suppress JA/Et pathway[58]
Bph32SCR-[59]
CC, coiled-coil domain; NB, nucleotide-binding domain; LRR, leucine-rich repeat domain; LRD, leucine-rich domain; LRK, lectin receptor kinase; SCR, short consensus repeat; SA, salicylic acid; JA, jasmonic acid; CK, cytokinin; Et, ethylene; BISP, BPH14-interacting salivary protein; NBR1, neighbor of BRCA1 gene 1 protein; SAMSL, S-adenosylmethionine synthetase-like protein.
Table 2. Identified N. lugens-associated elicitors and effectors.
Table 2. Identified N. lugens-associated elicitors and effectors.
NameCharacterizationFunctionRef.
NlMLPMucin-like proteinSalivary sheath formation; induce cell death, defense-related gene expression, and callose deposition in tobacco[75]
NlSP1Salivary protein 1Induce cell death, H2O2 accumulation, defense-related gene expression, and callose deposition in tobacco[76]
Nl12Disulfide isomeraseInduce cell death, defense-related gene expression, and callose deposition in tobacco[77]
Nl16Apolipophorin-IIIInduce cell death, defense-related gene expression, and callose deposition in tobacco[77]
Nl28Cysteine-rich proteinInduce cell death, defense-related gene expression, and callose deposition in tobacco[77]
Nl32Chemosensory
protein
Induce plant dwarfism, defense-related gene expression, and callose deposition in tobacco[77]
Nl40N. lugens-specific
salivary protein
Induce chlorosis, defense-related gene expression, and callose deposition in tobacco[77]
Nl43Uncharacterized
protein
Induce cell death, defense-related gene expression, and callose deposition in tobacco[77]
NlVgNN-terminal subunit
of vitellogenin
Induce cytosolic Ca2+ and H2O2 accumulation, JA and JA-Ile production, defense-related gene expression, and volatile release in rice[78]
NlDNAJB9DNAJ proteinInduce cell death, Ca2+ signaling, MAPK cascades, ROS accumulation, and callose deposition; activate JA pathway in tobacco[79]
NlG14A protein specific
to the salivary gland
Induce cell death, ROS accumulation, and callose deposition; activate JA pathway[80]
NlCSP11Chemosensory proteinInduce cell death, dwarfism, and SA-dependent systemic resistance against pathogens; interact with RCSP (TNL lacking catalytic Glu)[81]
NlEG1Endo-β-1,4-GlucanaseEnable N. lugens feeding; degrade celluloses in rice cell walls[82]
BISPBPH14-interacting salivary proteinTrigger BPH14-mediated resistance and activate NBR1-dependent selective autophagy[60]
NlSEF1EF-hand calcium-binding
protein
Suppress H2O2 and Ca2+ accumulation in rice[83]
CaMCalmodulinEnable N. lugens feeding, bind calcium, and suppress H2O2 accumulation and callose deposition in rice[84]
NIHSC70-3Heat shock 70 kDa protein cognate 3Suppress flg22-induced ROS bursts and defense-related gene expression in tobacco[85]
Nl1414-3-3e proteinInteract with enhanced disease resistance 1-like (OsEDR1l), suppress N. lugens-induced JA, JA-Ile and H2O2 accumulation, and facilitate N. lugens infestation[86]
NlugOBP11Odorant-binding proteinEnable N. lugens feeding and suppress SA pathway in rice[87]
miR-7-5PmicroRNATarget the immune-associated bZIP transcription factor (OsbZIP43) and suppress OsbZIP43-induced rice immunity[49]
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Zheng, X.; Wu, W.; Huang, Y.; Xu, K.; Shangguan, X. Mechanisms of Resistance of Oryza sativa to Phytophagous Insects and Modulators Secreted by Nilaparvata lugens (Hemiptera, Delphacidae) When Feeding on Rice Plants. Agronomy 2025, 15, 1891. https://doi.org/10.3390/agronomy15081891

AMA Style

Zheng X, Wu W, Huang Y, Xu K, Shangguan X. Mechanisms of Resistance of Oryza sativa to Phytophagous Insects and Modulators Secreted by Nilaparvata lugens (Hemiptera, Delphacidae) When Feeding on Rice Plants. Agronomy. 2025; 15(8):1891. https://doi.org/10.3390/agronomy15081891

Chicago/Turabian Style

Zheng, Xiaohong, Weiling Wu, Yuting Huang, Kedong Xu, and Xinxin Shangguan. 2025. "Mechanisms of Resistance of Oryza sativa to Phytophagous Insects and Modulators Secreted by Nilaparvata lugens (Hemiptera, Delphacidae) When Feeding on Rice Plants" Agronomy 15, no. 8: 1891. https://doi.org/10.3390/agronomy15081891

APA Style

Zheng, X., Wu, W., Huang, Y., Xu, K., & Shangguan, X. (2025). Mechanisms of Resistance of Oryza sativa to Phytophagous Insects and Modulators Secreted by Nilaparvata lugens (Hemiptera, Delphacidae) When Feeding on Rice Plants. Agronomy, 15(8), 1891. https://doi.org/10.3390/agronomy15081891

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