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Review

Recent Advances in the Genetic and Biochemical Mechanisms of Rice Resistance to Brown Planthoppers (Nilaparvata lugens Stål)

by
Shaojie Shi
1,†,
Huiying Wang
1,†,
Wenjun Zha
1,
Yan Wu
1,
Kai Liu
1,
Deze Xu
1,
Guangcun He
2,
Lei Zhou
1,3,* and
Aiqing You
1,3,*
1
Laboratory of Crop Molecular Breeding, Ministry of Agriculture and Rural Affairs, Hubei Key Laboratory of Food Crop Germplasm and Genetic Improvement, Food Crops Institute, Hubei Academy of Agricultural Sciences, Wuhan 430064, China
2
State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China
3
Hubei Hongshan Laboratory, Wuhan 430070, China
*
Authors to whom correspondence should be addressed.
†
These authors have contributed equally to this work.
Int. J. Mol. Sci. 2023, 24(23), 16959; https://doi.org/10.3390/ijms242316959
Submission received: 2 November 2023 / Revised: 26 November 2023 / Accepted: 27 November 2023 / Published: 30 November 2023
(This article belongs to the Special Issue New Insights into Plants and Insects Interactions)
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Abstract

:
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.

1. Introduction

The brown planthopper (Nilaparvata lugens Stål, BPH) is a host-specific herbivore that is widespread in Asia, Australia, and the South Pacific islands [1]. N. lugens soaks up phloem sap by inserting needle-like stylets into the vascular tissue of rice (Oryza sativa L.) [2]. Large amounts of BPHs often gathered in groups to harm plants, and caused wilting, yellowing, and even death of rice plants, as well as “hopperburn” in BPH-susceptible rice fields [3]. BPHs are also vectors of various viruses of rice, such as the grassy stunt virus and ragged stunt virus, which were introduced into rice plants during the N. lugens feeding process [4,5,6]. Direct and indirect economic losses induced by BPH feeding in Asia alone exceed hundreds of millions of dollars on an annual basis [7]. Brown planthoppers have become one of the most serious pests that harm rice production [3].
Currently, the application of chemical insecticides remains the major approach to controlling BPH in the field [8]. However, the widespread use of these compounds is hazardous to human health and the environment and has side effects that impact the natural enemies of BPH [9]. In addition, the indiscriminate use of pesticides can promote the emergence of insecticide resistance in BPHs [10,11]. Wu et al. found that the insecticide resistance to different insecticides (including imidacloprid, buprofezin, thiamethoxam, pymetrozine fufprole, chlorpyrifos, sulfoxafor, nitenpyram) of 69 N. lugens populations collected from eight Chinese provinces improved to varying degrees [12]. This led to a significant reduction in the toxicity efficiency against BPH [13,14,15,16]. Therefore, other BPH management strategies that are greener, healthier, and more sustainable must be developed. Utilizing the inherent resistance genes of rice to cultivate resistant rice varieties has been widely considered as the most cost-effective method for sustainable BPH control [17,18,19].
DNA sequence data show that the host of BPHs began to gradually transfer from Leersia to rice approximately 2.5 million years ago [1]. Rice has since evolved sophisticated defense systems to resist BPH infection, and BPHs have evolved various mechanisms to overcome these defenses [1]. Here, we review recent advances in research on the detection of BPH-resistance genes/QTLs, the mechanisms by which rice resists BPH infestations, and the roles of BPH secretory proteins in activating or suppressing rice defenses, and discuss their utilization in diminishing damage caused by brown planthoppers. Additionally, we discuss the research progress in N. lugens controlling methods. The insights from this review will enhance our understanding of the survival competition mechanism between rice and BPH and aid the development of strategies to establish green integrated BPH management.

2. BPH-Resistance Gene Mapping

The indica cultivar Mudgo, the first BPH-resistant rice germplasm, was identified in 1969 by the International Rice Research Institute [20]. Bph1, the first BPH-resistance gene identified from Mudgo, was mapped on chromosome 12 [21]. In recent decades, more than 49 BPH-resistance genes/QTLs have been detected due to the development of molecular marker technology and methods for evaluating the resistance of rice to BPHs [2,3,22,23,24]. Among these 49 genes/QTLs, 33 (Bph37 from IR64; Bph38(t), Bph33(t), bph19, Bph31, Bph44(t), qBph4.3, Bph33, Bph30, Bph41, Bph40, qBph4.1, Bph3, and qBph4.2 from IR65482-17, qBph4.4, Bph17, and qBph4.2 from Rathu Heenati; Bph27(t), Bph6, Bph44, Bph42, Bph25, and Bph37 from SE382; Bph32, bph4, Bph43, Bph28(t), bph2, bph7, and Bph9 from Kaharamana; and Bph1, Bph26, and Bph9 from Pokkali) were derived from traditional cultivated rice species; the rest were derived from wild rice varieties, including Bph13(t), bph11, qBph3, Bph14, qBph4, and Bph15 from O. officinalis; Bph12 from O. latifolia; Bph35, Bph36, Bph27, and bph29 from O. rufipogon; Bph21 and Bph20(t) from O. minuta; Bph34 from O. nivara; and Bph18 and Bph10 from O. australiensis (Table 1). Rice varieties containing one or more BPH-resistance genes/QTLs have been developed, and the cultivation of these varieties has greatly reduced the loss of rice yield induced by BPH feeding [25].
Most of the BPH-resistance genes/QTLs identified to date were located on six of twelve chromosomes (chromosomes 1, 3, 4, 6, 11, and 12), and their distribution on chromosomes was clustered (Figure 1). Three genes (bph11, qBph3, and Bph14) were clustered between 35.60 and 35.80 Mb of chromosome 3L [29,32,34]. A total of 21 genes were located on chromosome 4: five genes (Bph44(t), qBph4.3, Bph33, Bph30, and Bph41) were clustered between 0.17 and 1.10 Mb on chromosome 4S [2,24,35,36,37]; 11 genes (Bph40, Bph12, qBph4.1, Bph3, Bph35, qBph4.2, Bph15, Bph36, qBph4, Bph20(t), and Bph17) were clustered between 4.44 and 9.38 Mb on chromosome 4S [2,3,33,38,39,40,41,42,43,44]; and Bph27(t), Bph6, Bph44, Bph34, and Bph42 were clustered on chromosome 4L between 20.60 and 21.80 Mb [24,37,45,46,47]. The Bph37 that from SE382, Bph25, bph29, Bph32 and bph4 were present on chromosome 6S between 0.21 and 1.47 Mb [22,48,49,50,51]. The Bph43 and Bph28(t) genes were clustered between 16.79 and 16.96 Mb of chromosome 11L [23,52]. Some regions of these genes in the same cluster might overlap, indicating that these genes were not the same but were tightly linked, or that they were the same gene. These clustered genes might also constitute different alleles of the same gene that mediate responses to different BPH populations. In the same region on chromosome 12L, a total of eight BPH-resistance genes have been isolated. Sequence alignment revealed that these genes were alleles, and four allelotypes were identified. An assessment of the BPH resistance of the four allelotypes revealed that the resistance to BPH populations conferred by allelotypes of the same resistance gene varies [54].

3. Cloning and Mechanisms of BPH-Resistance Genes

A total of 17 BPH-resistance genes have been isolated to date (Table 2). These genes can be classified into seven types based on the types of encoded proteins. Coiled-coil, nucleotide-binding, and leucine-rich repeat (CC–NB–LRR, CNL) protein is encoded by Bph14 [34]. Bph1, Bph2, Bph7, Bph9, Bph10, Bph18, Bph21, Bph26, and Bph37 encode atypical CC–NB–LRR proteins [22,54,59]. Bph15 and Bph3 encode lectin receptor-like kinases (LecRKs) [39,60]. Leucine-rich repeat domain (LRD)-containing proteins are encoded by Bph30 and Bph40 [2]. Bph6 encodes an atypical LRR protein [46]. A B3 DNA-binding domain protein is encoded by bph29 [49]. Bph32 encodes a short consensus repeat (SCR) domain-containing protein [50]. The high variation in the types of proteins encoded by BPH-resistance genes reflected the high diversity in BPH-resistance mechanisms. These genes have been used to develop resistant rice varieties for the sustainable prevention and control of BPHs [25].

3.1. CC–NB–LRR Gene

Bph14 was the first BPH-resistance gene to be cloned. This gene was isolated from the highly resistant line B5, which is a chromosome fragment infiltration line derived from the wild rice species Oryza officinalis. Bph14 was first mapped on the long arm of chromosome 3 between markers R1925 and R2443 using the segregating population from the cross between B5 and Minghui 63 [3]. Du et al. fine-mapped Bph14 and ultimately located it within the 34 kb interval between molecular markers SM1 and G1318 [34]. Two candidate genes, Ra and Rb, are present in this region. Transgenic functional verification revealed that Ra was Bph14. Bph14 encodes a typical CNL protein, which is mainly accumulated in the vascular tissue. The salicylic acid (SA) signaling pathway was activated and callose deposition was induced in phloem during BPH feeding on plants expressing Bph14 [34]. Additional studies have shown that BPH14 interacts with the transcription factors (TFs) OsWRKY46 and OsWRKY72 and activates the expression of the receptor-like cytoplasmic kinase gene RLCK281 and the callose synthase gene LOC_Os01g67364.1 in rice [23].

3.2. Atypical CC–NB–LRR Genes

A rare CC–NB–LRR protein with two NB domains (CC–NB–NB–LRR, CNNL) was encoded by Bph9 [54]. Following BPH infestation, the SA signaling pathway was rapidly activated in plants expressing Bph9 [54]. The CC domain of BPH9 has been shown to confer resistance to attack from BPHs. The NB1 and NB2 domains in BPH9 protein have been shown to be essential for the resistance of BPH9 to BPHs. NB2 domain with the intact NB function motifs repressed the activation of the CC domain. However, the NB1 domain did not have this function, as its sequence differed greatly from the NB function motifs. The LRR domain is responsible for the activation of BPH9 during BPH infestation [23]. Bph9 was isolated from the indica rice variety Pokkali, and it was located in the interval on chromosome 12L between the markers InD2 and RsaI. The location of Bph9 overlapped with the position intervals of seven other BPH-resistance genes (Bph1, Bph2, Bph7, Bph10, Bph18, Bph21, and Bph26). Genomic sequence alignment and analyses of the chromosomal locations of these genes have shown that the aforementioned eight genes were allelic to each other. Four allelotypes could be classified according to their sequences, and they conferred varying levels of resistance to three brown planthopper populations [54].
Another unusual CC–NB–LRR protein that lacked the LRR domain and only contained CC and NB domains was encoded by Bph37 [22]. Bph37 was mapped between 1.20 and 1.57 Mbp on chromosome 6S. In this region, a typical CC–NB–LRR protein was encoded by LOC_Os06g03500 in the BPH-susceptible varieties Nipponbare and Kasalath. Whereas the premature termination of translation of LOC_Os06g03500 in BPH-resistance variety SE382 was due to one base inserted in the second exon, which explained the absence of the LRR domain. Functional verification indicated that LOC_Os06g03500 cloned from SE382 was Bph37 [22]. The isolation of Bph37 and studies of the domains of BPH14 and BPH9 suggest that the functions of the CC, NB, and LRR domains in BPH-resistance proteins may vary.

3.3. LRD Genes

Recently, the novel BPH-resistance gene Bph30, which encodes an LRD protein, was cloned from the cultivated rice variety AC-1613, and it was mainly expressed in the sclerenchyma cells of the rice leaf sheath [2]. BPH30 promotes the deposition of cellulose and hemicellulose in the sclerenchyma cell wall, which increases the cell wall stiffness and sclerenchyma thickness [2]. These structural changes impeded the ability of planthoppers to pierce the sclerenchyma with their stylets and feed on the phloem, thus conferring broad-spectrum resistance to planthoppers in rice [2]. Through the analysis of homologous genes and genome-wide association studies, the Bph30-like gene, Bph40, was isolated from the cultivated rice varieties SE232, SE67, and C334. Bph40 encodes an LRD protein that was identified as BPH30. BPH40 has been shown to promote the deposition of cellulose and hemicellulose in the sclerenchyma cell wall, which might be similar to the resistance mechanism of BPH30 [2]. A total of 27 Bph30-like genes that encode proteins containing LRDs were identified in the Nipponbare genome. Whether other Bph30-like genes confer resistance to BPHs remains unclear. Future studies of Bph30-like genes may provide additional genetic resources and aid the development of more efficient strategies for isolating new BPH-resistance genes [2].

3.4. LecRK Genes

Bph15 encodes an LecRK protein. This gene was derived from the resistant line B5, and it was initially mapped to a 0.4 cM interval on the short arm of chromosome 4 [3]. Next, a more refined genetic map was developed, and Bph15 was located in a 47 kb interval between markers RG1 and RG2 [3]. Bph15 from this region was isolated, and silencing this gene in rice weakened the anti-xenosis effect of BPHs [60]. Bph3 was mapped to a 79 kb interval on the short arm of chromosome 4 [39]. The isolation and characterization of Bph3 have indicated that Bph3 is actually a cluster of genes encoding three lectin receptor-like kinases (OsLecRK1–OsLecRK3) [39]. Individual genes or a combination of two genes only confer partial resistance to BPHs, whereas the presence of all three genes confers durable and broad-spectrum resistance to BPHs and WBPHs in rice [39]. BPH15 and BPH3 are all localized to the plasma membrane, indicating that these four proteins might be pattern recognition receptors that receive herbivory-associated molecular patterns [23].

3.5. Other Types of BPH-Resistance Genes

Bph6 encodes an atypical LRR protein [46]. This gene was initially mapped on the long arm of chromosome 4 between the simple sequence repeat (SSR) markers Y9 and Y19. It was derived from the Bangladesh landrace Swarnalata [3]. Guo et al. fine-mapped this gene and isolated it from the interval between the molecular markers H and Y9 [46]. BPH6 interacts with OsEXO70E1 and facilitates exocytosis [46]. Bph6 confers broad-spectrum resistance to planthoppers by reinforcing the cell wall and activating SA, jasmonic acid (JA), and cytokinin (CK) signaling [46]. Recent studies have shown that BPH6 interacts with OsEXO70H3 and S-adenosylmethionine synthetase-like protein (SAMSL), which facilitates SAMSL secretion to the apoplast, where it promotes lignin deposition in the cell wall [61].
bph29 is a recessive gene that was isolated from RBPH54. bph29 was previously positioned on chromosome 6S between markers RM435 and RM540 [62]. Subsequent studies reduced the mapping range of bph29 to 24 kb between markers BYL8 and BID2. A B3 DNA-binding domain protein is encoded by bph29. BPH infestation activates the SA signaling pathway, whereas it suppresses the JA/ethylene (ET) signaling pathway in RBPH54 [49]. Bph32 was initially identified between markers RM19291 and RM8072 on the short arm of chromosome 6. This region was approximately 170 kb and 190 kb in 9311 and Nipponbare, respectively. Bioinformatics and DNA sequence comparison mediated the isolation of Bph32 from Ptb33 [50]. Bph32 encodes a protein with an SCR domain, and this protein confers resistance to BPHs by antibiosis [50].

4. Responses of Rice to BPH Infection

The host of BPHs started shifting from Leersia to rice approximately 0.25 million years ago [1]. BPHs then began to feed specifically on rice plants [3]. Rice plants have evolved multiple mechanisms to resist attack from BPHs (Figure 2) [2,3,46]. Several studies have focused on clarifying the molecular mechanisms of BPH resistance, and these studies have enhanced our understanding of the responses of rice to BPH feeding [3,46].

4.1. MAPK Signal Transduction

Mitogen-activated protein kinases (MAPKs) are a group of very conservative protein kinases in eukaryotes [63,64]. The activation of MAPKs is an early reaction of plant exposure to biotic and abiotic stress [63]. Biochemical and genetic studies have revealed that MAPK cascades connect the different stimuli and downstream responses in plants [23]. Several OsMAPK genes have been shown to alter the defense gene expression or phytohormone levels to regulate the resistance of rice to BPHs. OsMAPK20-5 is a group D MAPK gene, and its expression was rapidly increased following female BPH infestation. BPH feeding increased the contents of ET and nitric oxide (NO) in OsMAPK20-5 silencing plants, which increased the BPH resistance of rice [64]. OsMKK3 was significantly induced after BPH infestation. The contents of JA, JA-Ile, and ABA were significantly increased, whereas the SA level was decreased in plants overexpressing OsMKK3 during BPH feeding, thus compromising the preference for BPH feeding, survival rate, and reproduction [65]. Nanda et al. showed that the expression of OsMPKs was remarkably influenced by BPH population type, rice variety, and infestation period [66]. OsSPL10 negatively regulated the resistance of rice against BPH. In spl10 mutant plants, genes related to the MAPK signaling pathway were remarkably upregulated during BPH feeding [67]. NlDNAJB9 is a BPH salivary protein that is highly expressed in salivary glands. In the NlDNAJB9 overexpression plants, MAPK cascades and other defense pathways were induced [68].

4.2. Phytohormones

Plant hormones play important roles in rice counteracting BPH. JA and SA are two of the most well-studied hormones involved in BPH resistance [69,70]. In Bph14-containing plants, BPH infestation increased SA content and the expression of SA-related genes, such as EDS1, NPR1, ICS1, PAL, and PAD4 [34]. Similar changes have been observed in Bph9- or bph29-containing plants following BPH feeding [49,54]. Exogenous spraying of SA increased the resistance level of rice to BPHs, suggesting that SA positively regulated BPH resistance [46]. It is generally believed that JA and SA are two antagonistic plant hormones that play opposite roles in the resistance of rice to phloem-sucking insects [61]. However, this might not always be the case. In plants expressing Bph6, SA, and JA seemed to participate in the resistance in a synergistic manner [46]. Recent studies have shown that JA-deficient mutants are susceptible to BPHs, and SA deficiency has no effect on BPH resistance [70]. These findings indicate that the functions of JA and SA in the response of rice to attack from BPHs might vary with genotypes and genetic backgrounds.
CK, ET, gibberellins (GA), brassinosteroids (BR), abscisic acid (ABA), and indoleacetic-3-acid (IAA) were also related to the rice defense against BPHs. In Bph6-containing plants, the CK content and the expression of synthetic genes increased substantially between 12 h and 24 h following BPH feeding, and the BPH resistance of plants was significantly increased after treatment with CKs [46]. ET is a defense phytohormone that has multiple impacts on insect infestations. OsACS2, the 1-aminocyclopropane-1-carboxylic acid (ACC) synthase gene, plays a role in herbivore-induced ET biosynthesis in rice. Knockdown of OsACS2 decreased the emission of ET and enhanced BPH resistance in rice [71]. The expression of OsGID1, a GA receptor gene in rice, was induced during BPH feeding. Overexpression of OsGID1 improved the BPH resistance level of rice, which was attributed to the increase in the level of lignin and the upregulation expression of three SA pathway-related WRKY genes (OsWRKY33, OsWRKY30, and OsWRKY13) [72]. Exogenous spraying of BR activated JA pathways and suppressed SA pathways, which increased the susceptibility of rice to BPHs [73]. ABA is a key phytohormone that is not only involved in the regulation of plant development but also in the responses to stress. Exogenous treatment with ABA enhanced callose synthase activity but suppressed β-1,3-glucanase activity, which inhibited BPH feeding [74]. Recent studies have shown that IAA negatively regulates the BPH resistance of rice plants [75].

4.3. Transcription Factors

The defense responses of rice against BPHs are usually accompanied by the regulation of defense-related gene expression and defense-associated signaling transduction, and TFs play important roles in regulating these processes [76]. The expression of OsWRKY45 was induced by BPH infestation and played a negative role in the BPH resistance of rice. In OsWRKY45-silenced plants, the content of H2O2 and ET was increased following BPH feeding, thus reducing the feeding, oviposition, and survival rate of BPH and delaying nymph development [77]. OsWRKY53 positively regulated BPH resistance by increasing H2O2 production during BPH infestation [78]. OsMYB30, an R2R3 MYB TF, directly upregulated the expression of OsPAL6 and OsPAL8, which encoded two key enzymes in the phenylalanine ammonia–lyase pathway and conferred BPH resistance in rice [69]. OsERF3 encodes an ethylene-responsive factor that reduces the BPH resistance of rice, which might stem from the decrease in the BPH-elicited H2O2 content [79]. The microarray and RNA sequencing results revealed significant differences in both the number and expression of differentially expressed TFs in resistant and susceptible materials following BPH feeding [80].

4.4. Metabolites

Changes in large amounts of metabolites, including primary metabolites, secondary metabolites, and defense compounds, have been observed in rice following BPH infestation [34,75,81]. The contents of amino acids, which are the main metabolites in phloem sap and essential nutrients for BPHs, were significantly reduced in BPH-resistance rice varieties during BPH feeding [75]. This might motivate BPHs to seek BPH-sensitive materials to acquire more nutritious sap [75]. Lipid profiles of rice leaf sheaths showed that the sterol biosynthetic pathway in the susceptible variety Nipponbare and wax biosynthesis and phytol metabolism in resistant Bph6-transgenic plants were activated during BPH feeding [61]. A recent study showed that Bph30 coordinated the flow of primary and secondary metabolites through the shikimate pathway, which conferred BPH resistance [75]. Serotonin is widespread in living organisms, and its synthesis was induced following BPH infestation. The suppression of serotonin biosynthesis increases levels of SA and enhances BPH resistance [81]. Schaftoside is a flavonoid that binds to the BPH CDK1 kinase NlCDK1 and affects its protein kinase activity, which reduces the survival of BPHs [82]. Callose is a well-studied compound involved in BPH resistance [23]. In BPH-resistant varieties, callose deposition blocked the phloem, which inhibited BPH feeding. In susceptible varieties, BPH infestation activated callose-hydrolyzing enzymes, which induced the degradation of callose and facilitated BPH feeding [34,46].

4.5. Calcium Signaling

Ca2+ is an important second messenger that is widespread in eukaryotes and plays a role in diverse biological processes [83]. Ca2+ influx was the earliest response of rice to BPH infestation [3]. NlSEF1, which is strongly expressed in the salivary glands of BPHs, encodes a Ca2+-binding protein that functions as an effector [84]. During BPH feeding, NlSEF1 is secreted into rice cells and decreases the cytosolic Ca2+ content, which is beneficial for the survival and feeding of BPHs [84]. This change in Ca2+ concentration is thought to function as a signal that elicits callose synthesis [61].

4.6. MicroRNAs

MicroRNAs (miRNAs) are single-stranded non-coding RNAs with a length of approximately 23 nt [85]. miRNAs bind target mRNAs through base complementary pairing to degrade them or inhibit translation, which mediates post-transcriptional gene silencing in both animals and plants [86]. Some studies have shown that miRNAs are involved in the responses of plants to external stimuli [87,88]. Wu et al. identified 23 miRNAs that were differentially expressed in Bph15 introgression plants (P15) and the susceptible recipient line 9311 (PC) prior to BPH feeding [89]. A total of 104 and 80 differentially expressed miRNAs were identified in P15 and PC, respectively, following BPH infestation [89]. Significant differences in the abundance and expression levels of differentially expressed miRNAs in BPH-resistance and susceptible varieties before and after BPH feeding have also been identified in several other studies [90,91]. OsmiR156, the main regulatory factor of individual plant development, negatively regulates the BPH resistance of rice by increasing levels of JA [92]. Dai et al. found that OsmiR396 silenced the expression of the OsGRF8, reducing the accumulation of transcripts of OsF3H and inhibiting flavonoid biosynthesis, thus negatively regulating BPH resistance in rice [93]. The results of these studies suggest that miRNAs play key roles in mediating the resistance of rice to BPHs. Additionally, these studies provided new target genes that could aid the breeding of BPH-resistance varieties.

5. BPH-Secreted Proteins That Involved in Rice–BPH Interactions

BPHs are typical piercing sucking insects that penetrate rice tissue with their stylets and suck phloem sap [94]. During the puncturing process, BPHs secrete a large number of proteins into rice tissues [95]. These secreted proteins are essential for the feeding success of BPHs and serve as key signaling molecules for initiating or suppressing rice immune responses (Figure 2) [96,97]. Several advances have been made in our understanding of BPH secretory proteins in recent years, and these studies have provided new insights into the interactions between rice and brown planthoppers [96,97,98].

5.1. BPH Elicitors

Elicitors are BPH secretory proteins that can be recognized by plants and trigger primary immune responses [99]. Mucin-like proteins are widespread in microorganisms [100]. NlMLP encodes an N. lugens-secreted mucin-like protein (NlMLP) identified from the BPH salivary glands [96]. During BPH feeding, NlMLP is secreted into rice tissues and induces rice defense responses, including the activation of the JA signaling pathway and MAP kinase, Ca2+ mobilization, and callose deposition [96]. NlMLP is indispensable for the assembly of stylet sheaths, and its silencing inhibits BPH feeding and performance [96]. Yolk proteins are crucial for egg development. The major precursors of yolk proteins, vitellogenins (Vgs), are usually cut into two segments [97]. NlVgN is the N-terminal subunit of the Vgs of BPHs and is present in saliva and eggs. The secretion of NlVgN into rice tissue induced direct defense responses, such as the production of JA-Ile, JA, cytosolic Ca2+, and H2O2, as well as indirect defense reactions, including the release of volatiles to attract female A. nilaparvatae wasps, which are natural enemies of BPHs. NlVg is also essential for the survival of BPHs, and disruptions in NlVg expression have a major effect on the feeding, development, and reproduction of BPHs [101]. N. lugens salivary protein 1 (NlSP1) was identified from the BPH salivary proteome. The secretion of NlSP1 into plants increases defense-related gene expression, H2O2 levels, and the deposition of callose [96].

5.2. BPH Effectors

Secretory proteins, known as effectors, can weaken defense responses [102,103]. NlEG1 was identified in salivary glands and encoded an endo-β-1,4-glucanase with endoglucanase activity. The silencing of NlEG1 reduced the ability of BPH stylets to puncture rice tissue. However, NlEG1 silencing had no effect on the ability of BPHs to consume an artificial diet. NlEG1 did not induce defense-related responses following its secretion into rice tissues via BPH feeding. These findings suggest that NlEG1 functions as an effector that reduces the resistance conferred by the cell wall [104]. The flavone tricin is widespread in rice plants and can enhance the resistance of rice to BPHs. Gong et al. identified an effector, BPH salivary protein 7 (NlSP7), and found that it decreased the tricin level in rice, which promoted BPH feeding [98]. In addition to suppressing immune responses, effectors can be recognized by specific resistance proteins, activating more intense immune responses [102,105]. The effector BPH14-interacting salivary protein (BISP) was identified in a recent study. BISP interacts with OsRLCK185, which attenuates its autophosphorylation to suppress basal defense responses. The BPH-resistance protein BPH14 can bind to BISP to activate other resistance pathways to stop BPH feeding [106].
In addition to being able to activate or inhibit the defense responses of rice, the aforementioned secreted elicitors and effectors are also indispensable for the feeding, development, and reproduction of BPHs. Therefore, these proteins may become new targets for controlling BPH.

6. Conclusions and Future Perspectives

To date, more than 49 BPH-resistance genes/QTLs have been identified, and the utilization efficiency of these genes in the breeding of BPH-resistance varieties has been low; this has resulted in the homogeneity of BPH-resistance genes in rice varieties [25]. The application of these BPH-resistant varieties will impose enormous selection pressure on BPH to favor the evolution of mechanisms to overcome these resistance genes [107]. BPH populations capable of overcoming the defenses conferred by common BPH-resistance genes have been observed in the laboratory [108,109]. There are several explanations for the lack of utilization efficiency of these BPH-resistance genes. First, the resistance levels of BPH-resistance genes derived from different donors were greatly affected by genetic backgrounds and environments, and this induced significant variation in resistance in rice varieties containing the same resistance gene. Second, traditional approaches for introducing genes are time-consuming and laborious. Few germplasm resources containing different types of BPH-resistance genes and excellent agronomic traits have been developed. Consequently, donor parents with high BPH resistance and good agronomic traits are lacking. Third, the aforementioned resistance genes are mostly incompletely dominant, and the BPH resistance of heterozygous individuals was weaker than that of homozygous individuals [2]; thus, more labor and time will be required for BPH-resistance breeding, especially for hybrid rice breeding. Fourth, the BPH resistance mechanisms remain unclear, which impedes the cultivation of varieties with broad-spectrum resistance and the efficacy of gene pyramiding. However, the discovery of novel types of BPH-resistance genes and defense mechanisms has facilitated major advances in the breeding of BPH-resistance rice varieties [2,46]. A series of BPH-resistance varieties have been cultivated using traditional and molecular-assisted breeding approaches, and this has aided efforts to control BPH populations and enhance rice yield [25].
BPH-susceptible genes and miRNAs in rice merit increased attention, especially in light of the rapid development of genetic engineering technology [110,111]. To date, few BPH susceptibility genes have been identified. OsERF3 plays a negative role in BPH resistance in rice by suppressing the biosynthesis of H2O2. The silencing of OsERF3 enhanced the BPH resistance of rice [79]. CYP71A1 is a cytochrome P450 gene. Knockout of CYP71A1 in rice plants blocked serotonin synthesis but increased SA levels, which enhanced BPH resistance [81]. OsACS2, which encodes an ACC synthase, negatively regulates BPH resistance. The silencing of OsACS2 increased the release of 2-heptanol and 2-heptanone, which are two repulsive volatiles, and suppressed BPHs infestation by attracting their natural enemy, Anagrus nilaparvatae [71]. Two miRNAs have also been identified to negatively regulate BPH resistance in rice [92,93]. Using genetic engineering methods to reshape the expression of these sensitive genetic materials, making BPH-susceptible varieties with excellent agronomic traits resistant is a fast and cost-effective breeding approach [112]. Although reprogramming these sensitive genetic materials may have deleterious effects on crop growth and yield, an improved understanding of BPH-resistance regulatory networks will greatly aid efforts to develop varieties that are resistant to BPHs without compromising yield [112].
Although studies of the mechanisms by which rice plants resist attack from BPHs can provide important insights that could aid the control of BPHs, studies of BPHs are also needed to achieve effective control of their populations. Many genomic, transcriptomic, and proteomic data on BPHs have been obtained in recent years, and several important elicitors and effectors have been discovered [96]. In addition to their roles in activating or inhibiting plant immunity, these proteins also play key roles in BPH feeding, and this merits increased research attention [96,97]. RNA interference can be used to silence target gene expression via double-stranded RNA (dsRNA) [113]. Although there are several challenges associated with the use of dsRNA, including its low stability in the environment, low absorption efficiency, and low intracellular delivery efficiency, dsRNA insecticides provide a green approach that could be effective for controlling infestations of insect pests [112,114,115,116,117]. This novel type of biopesticide has been used to control various diseases of plants in a sustainable and eco-friendly manner [118,119,120,121,122]. A system that co-delivers insecticide and dsRNA was recently developed that could be used to silence insecticide resistance genes in pests, which would increase the susceptibility of insect herbivores to insecticides [114,123,124,125]. This provides an optional approach for BPH control.
In addition, other environmentally friendly strategies for BPH management should also be considered. Cultural management is a simple and important eco-friendly method for controlling BPH, although it might not provide immediate results [107]. Crop rotation plays a significant role in restricting population of BPH. For instance, rotating rice with non-host plants or BPH-resistant varieties can remarkably decrease BPH populations [107]. Trap cropping is a useful strategy for BPH control and is commonly used in Asian countries [126]. Trap plants grow together with the major crop, attracting pests away from the major crop or attracting natural enemies, thereby protecting the main plants from pests [126,127,128]. One study showed that highly susceptible rice plants that were planted 20 d earlier around the main rice field attracted a large number of BPHs to feed, thus reducing the population on the major crop [126]. The pulling power of trap plants, planting time, and required space should be comprehensively considered before choosing trap crops [126]. Biological control, in which natural enemies such as predators and parasitoids play a major role, is another eco-friendly method for rectifying the harm of BPHs [107]. Predators of eggs, such as Cyrtorhinus lividipennis, larvae predators, including Cyrtorhinus lividipennis, Lycosa. Pseudoannulata, and Migrovelia douglasi, and predators of both larvae and adults, such as Synharmoni octomaculata (F.) and Paederus fuscipes Curtis, were found to significantly decrease BPH populations [129,130]. The parasitoids, such as Oligosita yasumatsui, Anagrus spp., and Pseudogonatopus spp. were also identified and considered indispensable factors in the biological control of BPHs [129,131].
In summary, the introduction of major BPH-resistance genes into rice varieties remains the most important method for BPH control. However, studies of the BPH resistance mechanisms of rice and improvements in genetic engineering technologies, as well as changes in agricultural practices will facilitate the development of a green tridimensional defense system to control BPH populations.

Author Contributions

Conceptualisation, A.Y., L.Z., S.S. and H.W.; writing—original draft preparation, S.S., H.W. and W.Z.; writing—review and editing, S.S., H.W., W.Z., Y.W., K.L., D.X., G.H., L.Z. and A.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This review was supported by grants from the Wuhan Knowledge Innovation Special Dawn Plan Project (2022020801020342), the Natural Science Foundation of Hubei Province (2022CFB832), the Hubei Academy of Agricultural Science Foundation (2023NKYJJ01), the Hubei Key Laboratory of Food Crop Germplasm and Genetic Improvement Foundation (2022lzjj01), the National Natural Science Foundation of China (32301855), the Science and Technology Major Program of Hubei Province (2022ABA001, 2021ABA011), and the Wuhan Science and Technology Major Project for Biological Breeding (2022021302024850).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data have been included in the manuscript.

Acknowledgments

We thank Shengli Jing (Xinyang Normal University) for kindly revising the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Ijms 24 16959 g001
Figure 1. Distribution of BPH-resistance genes/QTLs on rice chromosomes. Numbers on the left indicate the physical distance. Black bars represented the position of BPH-resistance genes/QTLs on rice chromosomes. Red represents genes that have been cloned, and black represents genes that have not been cloned.
Figure 1. Distribution of BPH-resistance genes/QTLs on rice chromosomes. Numbers on the left indicate the physical distance. Black bars represented the position of BPH-resistance genes/QTLs on rice chromosomes. Red represents genes that have been cloned, and black represents genes that have not been cloned.
Ijms 24 16959 g001
Ijms 24 16959 g002
Figure 2. Model of rice-brown planthopper interactions. During BPH feeding on rice, elicitors and effectors were secreted into rice cells. Elicitors are perceived by PRRs, activating basic immune responses, such as elevated levels of ROS. However, effectors suppress the first-layer immune responses, such as BISP, which interacts with OsRLCK185 and suppresses its phosphorylation. The BPH-resistance proteins recognize these effectors, triggering second-layer immune reactions, including the activation or suppression of phytohormone signaling pathways and enhancement of the cell wall of leaf sheaths, thus inhibiting BPH from sucking phloem sap. ROS, reactive oxygen species; SA, salicylic acid; JA, jasmonic acid; CK, cytokinin; IAA, indole-3-acetic acid.
Figure 2. Model of rice-brown planthopper interactions. During BPH feeding on rice, elicitors and effectors were secreted into rice cells. Elicitors are perceived by PRRs, activating basic immune responses, such as elevated levels of ROS. However, effectors suppress the first-layer immune responses, such as BISP, which interacts with OsRLCK185 and suppresses its phosphorylation. The BPH-resistance proteins recognize these effectors, triggering second-layer immune reactions, including the activation or suppression of phytohormone signaling pathways and enhancement of the cell wall of leaf sheaths, thus inhibiting BPH from sucking phloem sap. ROS, reactive oxygen species; SA, salicylic acid; JA, jasmonic acid; CK, cytokinin; IAA, indole-3-acetic acid.
Ijms 24 16959 g002
Table 1. BPH-resistance genes/QTLs discovered in rice.
Table 1. BPH-resistance genes/QTLs discovered in rice.
GeneGermplasmChromosomeLinked MarkersReference
Bph37IR641LRM302, YM35[26]
Bph38(t)Khazar1L693369, id1012165[27]
Bph33(t)RP20681LRM488, RM11522[28]
Bph13(t)O. officinalis3SAJ09b, AJ09c[29]
bph19AS20-13SRM6308, RM3134[30]
Bph31CR2711-763LPA26, RM2334[31]
bph11O. officinalis3LG1318[32]
qBph3IR02W101 (O. officinalis)3Lt6, f3, c3-14[33]
Bph14B5 (O. officinalis)3LSM1, G1318[34]
Bph44(t)IRGC 153444S344-0-6, 344-1-2[24]
qBph4.3Salkathi4SRM551, RM335[35]
Bph33Kolayal, Poliyal4SH99, H101[36]
Bph30AC-16134SSSR28, SSR69[2]
Bph41SWD104SSWRm_01617, SWRm_01522[37]
Bph40SE232, SE67, C3344S-[2]
Bph12O. latifolia4SRM16459, RM1305[3]
qBph4.1Rathu Heenati4S-[38]
Bph3Rathu Heenati4SRHD9, RHC10[39]
Bph35RBPH660 (O. rufipogon)4SPSM16, R4M13[40]
qBph4.2IR65482-174SRM261, S1, XC4-27[41]
Bph15B5 (O. officinalis)4SRG1, RG2[3]
qBph4.4Salkathi4SRM335, RM5633[35]
Bph36O. rufipogon4LS13, X48[42]
qBph4IR02W101 (O.officinalis)4Sp17, xc4-27[33]
Bph20(t)O. minuta4SB42, B44[43]
Bph17Rathu Heenati4SRM8213, RM5953[44]
qBph4.2Rathu Heenati4L-[38]
Bph27O. rufipogon4LRM16766, RM17033[42]
Bph27(t)Balamawee4LQ52, Q20[45]
Bph6Swarnalata4LH, Y9[46]
Bph44Balamawee4LQ31, RM17007[24]
Bph34O. nivara4LRM16994, RM17007[47]
Bph42SWD104LSWRm_01695, SWRm_00328[37]
Bph25ADR526SS00310[48]
bph29O. rufipogon6SBYL8, BID2[49]
Bph37SE3826S-[22]
Bph32Ptb336SRM19291, RM8072[50]
bph4Babawee6SRM190, C76A[51]
Bph43IRGC 867811L16-22, 16-30[23]
Bph28(t)DV8511LIndel55, Indel66[52]
bph2ASD712LRM7102, RM463[53]
bph7T1212LRM3448, RM313[54]
Bph10O. australiensis12LRG457[55]
Bph9Kaharamana12LRM463, RM5341[56]
Bph1Mudgo12Lem5814N, em2802N[57]
Bph26ADR5212LDS72B4, DS173B[58]
Bph18O. australiensis12LBIM3, BN162[59]
Bph9Pokkali12LInD2, RsaI[54]
Bph21O. minuta12LS12094A, B122[43]
S, short arm of chromosome; L, long arm of chromosome.
Table 2. BPH-resistance genes isolated from rice.
Table 2. BPH-resistance genes isolated from rice.
GeneGermplasmChromosomeEncoded ProteinDefense MechanismReference
Bph14B53LCC-NB-LRRSA↑, callose deposition[34]
Bph9Pokkali12LCC-NB-NB-LRRSA↑[54]
Bph1Mudgo12LCC-NB-NB-LRR-[54]
Bph2ASD712LCC-NB-NB-LRR-[54]
bph7T1212LCC-NB-NB-LRR-[54]
Bph10IR65482-4-136-2-212LCC-NB-NB-LRR-[54]
Bph18IR65482-7-216-1-212LCC-NB-NB-LRR-[59]
Bph21IR71033-121-1512LCC-NB-NB-LRR-[54]
Bph26ADR5212LCC-NB-NB-LRR-[58]
Bph37SE3826SCC-NB-[22]
Bph6Swarnalata4LAtypical LRRSA↑, JA↑, CK↑, enhanced cell walls[46]
Bph30AC-16134SLRDenhanced cell walls, IAA↓[2]
Bph40SE232, SE67, C3344SLRDenhanced cell walls[2]
Bph15B54SLectin receptor
kinase		OsPR1a↑, OsLOX↑, OsCHS↑[60]
Bph3Rathu Heenati4SLectin receptor
kinase		-[39]
bph29RBPH546SB3 DNA-bindingSA↑, JA/ET↓[49]
Bph32PTB336SSCR-[50]
S, short arm of chromosome; L, long arm of chromosome; CC, coiled coil domain; NB, nucleotide-binding domain; LRR, leucine-rich repeat domain; LRD, leucine-rich domain; SCR, short consensus repeat; SA, salicylic acid; JA, jasmonic acid; CK, cytokinin; IAA, indole-3-acetic acid; ET, ethylene; ↑, up-regulation; ↓, down-regulation.
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Shi, S.; Wang, H.; Zha, W.; Wu, Y.; Liu, K.; Xu, D.; He, G.; Zhou, L.; You, A. Recent Advances in the Genetic and Biochemical Mechanisms of Rice Resistance to Brown Planthoppers (Nilaparvata lugens Stål). Int. J. Mol. Sci. 2023, 24, 16959. https://doi.org/10.3390/ijms242316959

AMA Style

Shi S, Wang H, Zha W, Wu Y, Liu K, Xu D, He G, Zhou L, You A. Recent Advances in the Genetic and Biochemical Mechanisms of Rice Resistance to Brown Planthoppers (Nilaparvata lugens Stål). International Journal of Molecular Sciences. 2023; 24(23):16959. https://doi.org/10.3390/ijms242316959

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Shi, Shaojie, Huiying Wang, Wenjun Zha, Yan Wu, Kai Liu, Deze Xu, Guangcun He, Lei Zhou, and Aiqing You. 2023. "Recent Advances in the Genetic and Biochemical Mechanisms of Rice Resistance to Brown Planthoppers (Nilaparvata lugens Stål)" International Journal of Molecular Sciences 24, no. 23: 16959. https://doi.org/10.3390/ijms242316959

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