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Identification and knockout of a herbivore susceptibility gene enhances planthopper resistance and increases rice yield

Nature Food (2024)Cite this article

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Abstract

Brown planthoppers (Nilaparvata lugens) and white-backed planthoppers (Sogatella furcifera) are among the most destructive pests on rice. However, plant susceptibility genes have not yet been exploited for crop protection. Here we identified a leucine-rich repeat protein, OsLRR2, from susceptible rice varieties that facilitates infestation by brown planthopper N. lugens. Field trials showed that knockout of OsLRR2 significantly reduced BPH infestation and enhanced natural biological control by attracting natural enemies. Yield of a susceptible variety was increased by 18% in insecticide-treated plots that eliminated planthoppers and by 25% in untreated plots. These findings underscore the pivotal role of OsLRR2, offering a promising pathway for pest population suppression and rice yield increase.

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Fig. 1: Subcellular localization and expression patterns of OsLRR2.
Fig. 2: Knockout of OsLRR2 enhances rice resistance to planthoppers in the glasshouse.
Fig. 3: OsLRR2 competitively binds to OsSERK1 and OsSERK2 reducing receptor–co-receptor complex formation.
Fig. 4: OsLRR2 regulates defence-related MPKs and phytohormone levels.
Fig. 5: OsLRR2 affects the production of defensive compounds.
Fig. 6: Knockout of OsLRR2 increases rice planthopper resistance and yield production in the field.

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Data availability

Sequence data from this paper can be found in the GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and Rice Genome Annotation Project (http://rice.uga.edu/index.shtml) data libraries under accession numbers: OsLRR2 (XM_015760400.2), OsSERK1 (LOC_Os08g07760), OsSERK2 (LOC_Os04g38480), OsSERK3 (LOC_Os06g12120), OsSERK4 (LOC_Os02g18320), OsFLS2 (LOC_Os04g52780), OsPEPR1 (LOC_Os08g34640), OsBRI1 (LOC_Os01g52050), OsMPK3 (LOC_Os03g17700), OsMPK4 (LOC_Os10g38950), OsMPK6 (LOC_Os06g06090), OsWRKY30 (LOC_Os08g38990), OsWRKY33 (LOC_Os03g33012), OsWRKY45 (LOC_Os05g25770), OsWRKY53 (LOC_Os05g27730), OsWRKY62 (LOC_Os09g25070), OsWRKY70 (LOC_Os05g39720), OsWRKY89 (LOC_Os11g02520), OsAOS1 (LOC_Os03g55800), OsOPR3 (LOC_Os08g35740), OsJAZ8 (LOC_Os09g26780), OsPR10a (LOC_Os12g36880), OsPR10b (LOC_Os12g36850), OsPR1a (LOC_Os07g03710), OsACS2 (LOC_Os04g48850), OsEBF1 (LOC_Os06g40360), OsNCED3 (LOC_Os03g44380), OsABI5 (LOC_Os01g64000), OsACTIN (LOC_Os03g50885) and OsUbi (LOC_Os03g13170). All data supporting the findings of this study are available in the article, supplementary information and source data files. Source data are provided with this paper.

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Acknowledgements

We thank H. Tong (Chinese Academy of Sciences) for providing seeds of OsSERK2 overexpression and knockout rice lines, F. Song (Zhejiang University) for providing the M. oryzae strain RB22, Y. Bi (Zhejiang University) for help with M. oryzae punch inoculation assays, H. Lu (Zhejiang University) for the gift of pHun4c12s vector, G. Dong (Zhejiang University) and L. Xie (Zhejiang University) for their assistance with plant growth and insect rearing and S. Jing, Y. Xu, Q. Gao, W. Xiao, X. Wang, J. Kong, C. Zhang and X. Luo (all from Zhejiang University) for their help with experiments. We thank M. Erb (University of Bern) for helpful comments and input. This study was financed by the National Natural Science Foundation of China (grant numbers 31930091 to Y.L. and 32202396 to P.K.), the National Program of Transgenic Variety Development of China (2022ZD0400301-3 to Y.L.), the Earmarked Fund for China Agriculture Research System (CARS-01-43 to Y.L.) and the Zhejiang Provincial Natural Science Foundation (LY24C140003 to P.K.).

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Author notes

  1. These authors contributed equally: Peng Kuai, Na Lin.

Authors and Affiliations

  1. State Key Laboratory of Rice Breeding and Biology and Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Insect Sciences, Zhejiang University, Hangzhou, China

    Peng Kuai, Na Lin, Miaofen Ye, Meng Ye, Lin Chen, Shuting Chen, Hongyue Zu, Lingfei Hu & Yonggen Lou

  2. School of Natural and Environmental Sciences, Newcastle University, Newcastle, UK

    Angharad M. R. Gatehouse

  3. Hainan Institute, Zhejiang University, Sanya, China

    Yonggen Lou

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  1. Peng Kuai
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  4. Meng Ye
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Contributions

P.K. and Y.L. designed the research; P.K., N.L., Miaofen Ye, Meng Ye, L.C., S.C., H.Z. and L.H. performed experiments; P.K., N.L. and Miaofen Ye analysed the data; P.K. and Y.L. prepared and wrote the article; A.M.R.G. critically commented and helped write the paper. All authors have read and agreed to the published version of the paper.

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Correspondence to Angharad M. R. Gatehouse or Yonggen Lou.

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Extended data

Extended Data Fig. 1 Overexpression of OsLRR2 in rice decreases plant resistance to planthoppers.

a−c) The egg number (laid by 15 gravid females for 12 h) (a), developmental duration (b) and hatch rate (c) of BPH eggs on oe-LRR2 lines and WT plants. Data are presented as mean values ± s.e.m., n = 8 biological replicates. Asterisks in (b) indicate significant differences in oe-LRR2 lines compared with WT plants evaluated by Bayesian analysis of variance (**P < 0.01). d,e) Number of gravid BPH females per plant on pairs of plants (a WT plant versus an oeLRR2-3 or oeLRR2-4 plant). Inserts: Percentage of BPH eggs per plant on pairs of plants as stated above, 48 h after the release of BPH. Data are presented as mean values + s.e.m., n = 8 biological replicates. Asterisks indicate significant differences in oe-LRR2 line compared with WT plants evaluated by two-sided Student’s t-test (*P < 0.05, **P < 0.01, and ***P < 0.001). f) Damage levels of oe-LRR2 and WT plants individually infested with 25 gravid BPH females for 10 days, n = 8 individual plants. Bars, 10 cm. g) Number of Anagrus nilaparvatae females attracted by volatiles emitted from WT and oe-LRR2 (oeLRR2-3 (#3) or oeLRR2-4 (#4)) plants that were infested with gravid BPH females for 48 h or non-infested plants. Pie chart indicates the number of A. nilaparvatae females that make a choice or not within 5 min. Asterisks indicate significant differences in oe-LRR2 lines compared with WT plants evaluated by Chi-squared test (*P < 0.05). For P values, see source data. Experiments were repeated at least twice with similar results.

Source data

Extended Data Fig. 2 Both OsSERK1 and OsSERK2 interact with OsLRR2 and three defence- or growth-related receptors, OsPEPR1, OsFLS2 and OsBRI1.

a) Pull-down of MBP-OsLRR2 by GST-OsSERK1 or GST-OsSERK2 in vitro. Key: GST, glutathione S-transferase; MBP, maltose-binding protein. Fusion proteins were immunodetected using anti-GST or anti-MBP antibody. b) Bimolecular fluorescence complementation (BiFC) assays confirmed the interaction between OsSERK1 and OsLRR2 and between OsSERK2 and OsLRR2 in Nicotiana benthamiana leaves. Co-expression of OsLRR2-fused N-terminal part of yellow fluorescent protein (OsLRR2-nYFP)/OsSERK1-fused C-terminal part of YFP (OsSERK1-cYFP), or OsLRR2-nYFP/OsSERK2-cYFP, but not nYFP (empty vector, EV)/OsSERK1-cYFP or nYFP/OsSERK1-cYFP or OsLRR2-nYFP/cYFP (empty vector), resulted in strong fluorescence signals. Bars, 20 μm. c) OsSERK1 interacts with OsLRR2 via the extracellular LRR domain in a yeast two hybrid (Y2H) assay. Schematic diagrams of the domain structure of OsLRR2 and OsSERK1 are indicated. Key: SP, signal peptide; LRR, extracellular leucine-rich repeat domain; TM, transmembrane domain; ICD, intracellular domain; OsSERK1LRR, the extracellular LRR domain of OsSERK1; OsSERK1ICD, the intracellular kinase domain of OsSERK1, and OsSERK1ΔSPTM, OsSERK1 without the signal peptide and transmembrane region; OsLRR2ΔSP, OsLRR2 without the signal peptide; Bait, protein with binding domain; Prey, protein with activation domain; EV, empty vector; SD/−2, synthetic dropout (SD) media lacking leucine and tryptophan; SD/−4, SD media lacking leucine, tryptophan, histidine and adenine; X-α-gal, 5-Bromo-4-chloro-3-indoxyl-α-D-galactopyranoside. Yeast (Saccharomyces cerevisiae) transformants expressing combinations of the OsLRR2ΔSP/OsSERK1ΔSPTM and OsLRR2ΔSP/OsSERK1LRR grow well on the synthetic dropout (SD)/−4 plate and exhibit activated β-galactosidase reporter activity (blue colour), whereas the transformants expressing OsLRR2ΔSP/OsSERK1ICD did not. d) Schematic diagrams of the domain structure of receptors used in the assay. Key: eJM, extracellular juxtamembrane; iJM, intracellular juxtamembrane; JMK, eJM+TM+iJM+ICD. e−g) Pull-down assays show that OsSERK1 and OsSERK2 bind to the extracellular LRR domain and the JMK domain of OsPEPR1 (e), OsFLS2 (f) or OsBRI1 (g). h−j) Addition of MBP protein (12 μg) does not influence binding of OsPEPR1LRR (h), OsFLS2LRR (i), or OsBRI1LRR (j) to OsSERK1 or OsSERK2. Experiments were repeated twice with similar results.

Source data

Extended Data Fig. 3 OsLRR2 negatively regulates defence responses of rice elicited by flg22 and resistance to rice blast.

a−d) The transcript levels of four marker genes related to OsFLS2-mediated rice defence, OsWRKY45 (a), OsPR1a (b), OsPR10a (c), and OsPR10b (d) in leaves of kolrr2-3, wild-type (WT) and oeLRR2-3 plants 1 h after treatment with 1 μM flg22 or mock (RNase-free water). Data are presented as mean values + s.e.m., n = 4 biological replicates. Asterisks in (a−d) indicate significant differences in kolrr2-3 or oeLRR2-3 lines compared with WT plants evaluated by two-sided Student’s t-test (*P < 0.05, **P < 0.01, and ***P < 0.001). e) Ko-lrr2, oe-LRR2 and wild-type (WT) plants showing different resistance to rice blast. Leaves were photographed at 5 d post inoculation with the Magnaporthe oryzae virulent strain RB22. Bar, 1 cm. f,g) The lesion length (f) and relative fungal biomass (g) were measured at 5 d post inoculation. Data are presented as mean values + s.e.m., n = 5 replications each with 12−21 independent lesions in (f) and n = 5 biological replicates in (g). Asterisks in (f,g) indicate significant differences in ko-lrr2 or oe-LRR2 lines compared with WT plants evaluated by Bayesian analysis of variance (***P < 0.001). For P values, see source data. RT-qPCR assays were repeated twice with similar results and disease resistance assays were repeated five times with similar results.

Source data

Extended Data Fig. 4 OsLRR2 negatively regulates the activation and/or transcript level of mitogen-activated protein kinases (MPKs) in plants.

a,b) The relative kinase activation of OsMPK6 (a) and OsMPK4 (b) in ko-lrr2 and WT plants based on signal intensity in four repeated experiments (relating to Fig. 4a and Supplementary Fig. 6a−c). The relative activation/quantification of all samples at each time point is expressed relative to the WT sample at 0 h (set to 1). Data are presented as mean values + s.e.m., n = 4 biological replicates. c−e) Transcript levels of OsMPK4 (c), OsMPK3 (d) and OsMPK6 (e) in ko-lrr2 and WT plants 0, 3, 8 and 12 h post infestation by gravid brown planthopper (BPH) females. Data are presented as mean values + s.e.m., n = 5 biological replicates. f) MPK activation in oe-LRR2 and WT plants 0, 1, 3, 8 and 12 h post infestation by gravid BPH females. g,h) The relative kinase activation of OsMPK6 (g) and OsMPK4 (h) in oe-LRR2 and WT plants based on signal intensity in three repeated experiments (relating to Supplementary Fig. 6d, e). Data are presented as mean values + s.e.m., n = 3 biological replicates. Asterisks in (a−d,g,h) indicate significant differences in ko-lrr2 or oe-LRR2 lines compared with WT plants at indicated times evaluated by Bayesian analysis of variance (*P < 0.05, **P < 0.01, and ***P < 0.001). For P values, see source data. Experiments were repeated twice with similar results.

Source data

Extended Data Fig. 5 Knocking out OsLRR2 influences transcript levels of defence-related WRKYs and genes related to phytohormone pathways but not salicylic acid levels in rice.

a−f) The transcript levels of defence-related WRKYs, OsWRKY53 (a), OsWRKY62 (b), OsWRKY70 (c), OsWRKY89 (d), OsWRKY30 (e), and OsWRKY33 (f) in ko-lrr2 and WT plants 0, 3, 8 and 12 h post infestation by gravid brown planthopper (BPH) females. g−n) The transcript levels of genes related to JA- (OsAOS1 (g), OsOPR3 (h), OsJAZ8 (i), and OsPR10a (j)), ABA- (OsNCED3 (k) and OsABI5 (l)), and ethylene- (OsACS2 (m) and OsEBF1 (n)) mediated signalling pathways in ko-lrr2 and WT plants 0, 3, 8 and 12 h post infestation by gravid BPH females. o) Levels of salicylic acid (SA) in ko-lrr2 and WT plants 0, 8, 24 and 48 h post infestation by gravid BPH females. Key: FM, fresh mass. Data in (a−o) are presented as mean values + s.e.m., n = 5 biological replicates, except for kolrr2-1 lines at 12 h post infestation in (c) (n = 4 biological replicates). Asterisks in (a−n) indicate significant differences in ko-lrr2 lines at indicated times compared with WT plants evaluated by Bayesian analysis of variance (*P < 0.05, **P < 0.01, and ***P < 0.001). For P values, see source data. Experiments were repeated twice with similar results.

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Extended Data Fig. 6 Overexpression of OsLRR2 in rice decreases levels of phytohormones in plants.

a−d) Levels of jasmonic acid (JA; a), JA-isoleucine (JA-Ile; b) and abscisic acid (ABA; c) and salicylic acid (SA; d) in oe-LRR2 lines and wild-type (WT) plants at different time points post infestation by gravid brown planthopper (BPH) females. e) Accumulated amounts of ethylene emitted from oe-LRR2 and WT plants that were individually infested with 15 gravid BPH females. Key: FM, fresh mass. Data are presented as mean values + s.e.m., n = 5 biological replicates in (a−d) and n = 6 biological replicates in (e). Asterisks indicate significant differences in oe-LRR2 lines at indicated times compared with WT plants evaluated by Bayesian analysis of variance (*P < 0.05, **P < 0.01, and ***P < 0.001). For P values, see source data. Experiments were repeated twice with similar results.

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Extended Data Fig. 7 OsSERK1 positively regulates rice resistance to brown planthoppers (BPH).

a−c) The egg number (laid by 15 gravid BPH females for 12 h) (a), egg developmental duration (b), and egg hatch rate (c) of BPH on oe-SERK1, as-serk1 and wild-type (WT, XS110) plants. Data are presented as mean values + s.e.m., n = 10 biological replicates. Asterisks in (b,c) indicate significant differences in transgenic lines compared with WT plants evaluated by Bayesian analysis of variance (**P < 0.01 and ***P < 0.001). d) Growth phenotypes of oe-SERK1, as-serk1 and WT (XS110) plants 8 d or 11 d after they were individually infested by 25 gravid BPH females, n = 8 individual plants. Bars, 10 cm. For P values, see source data. Experiments were repeated twice with similar results.

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Extended Data Fig. 8 Effects of knocking out OsLRR2 on the population density of planthoppers and their main predators, and rice yield parameters in rice fields.

a,b) Number of adults of white-backed planthopper (WBPH) (a) or brown planthopper (BPH) (b) per plant of ko-lrr2 and wild-type (WT) lines. c,d) Number of spiders (c) and green mirid bugs (d) per plant of ko-lrr2 and wild-type (WT) lines. In (a−d), data are presented as mean values + s.e.m., n = 3 individual plots, each plot collected from 15 hill plants. e,f) The seed setting rate (e) and 1,000-grain weight (f) of ko-lrr2 and WT lines in the pest-infested or pest-controlled field. In (e,f), data are presented as mean values + s.e.m., n = 3 individual plots, each plot collected from 10 hill plants in the pest-infested fields or 5 hill plants in the pest-controlled fields. g) Mature grain of ko-lrr2 and WT rice plants in the pest-infested or pest-controlled field. Bars, 1 cm. h,i) The 10-grain length (h) and 10-grain width (i) of ko-lrr2 and WT rice lines in the pest-infested or pest-controlled field. Data are presented as mean values + s.e.m., n = 10 biological replicates. Asterisks in (a,b,f,h,i) indicate significant differences in ko-lrr2 lines compared with WT plants evaluated by Bayesian analysis of variance (*P < 0.05, **P < 0.01, and ***P < 0.001). For P values, see source data.

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Extended Data Fig. 9 Effects of knocking out OsLRR2 in variety XS11 on rice yield parameters in the field in 2021 and 2024.

a) Growth phenotypes of ko-lrr2 lines and wild-type (WT) plants at maturity in the field. Bars, 10 cm. b−e) The grain yield per plant (b), number of panicles per plant (c), seed setting rate (d) and 1,000-grain weight (e) of ko-lrr2 and WT lines in the pest-controlled field in Changxing, Zhejiang in 2021 and in Sanya, Hainan in 2024. Data in (b−e) are presented as mean values + s.e.m., n = 3 individual plots, each plot collected from 5 hill plants. f,g) The 10-grain length (f) and 10-grain width (g) of ko-lrr2 and WT lines in the pest-controlled field in Changxing, Zhejiang in 2021 and in Sanya, Hainan in 2024. Data in (f,g) are presented as mean values + s.e.m., n = 15 biological replicates. h) Mature grain of ko-lrr2 and WT rice plants in the field. Bars, 1 cm. Asterisks in (b,c,e−g) indicate significant differences in ko-lrr2 lines compared with WT plants evaluated by Bayesian analysis of variance (**P < 0.01 and ***P < 0.001). For P values, see source data.

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Extended Data Fig. 10 Knocking out OsLRR2 in rice variety Xiushui110 (XS110) enhances rice resistance to planthoppers and grain size in the field.

a−c) The egg number (laid by 15 gravid females for 12 h) (a), egg developmental duration (b) and egg hatch rate (c) of brown planthopper (BPH) on ko-lrr2 and wild-type (WT, XS110) plants. Data are presented as mean values ± s.e.m., n = 10 biological replicates. Asterisks in (b,c) indicate significant differences in ko-lrr2 lines compared with WT (XS110) plants evaluated by Bayesian analysis of variance (***P < 0.001). d,e) Number of gravid BPH females per plant on pairs of plants (a WT plant versus an kolrr2-9 or kolrr2-18 plant). Inserts: Percentage of BPH eggs per plant on pairs of plants as stated above, 48 h after the release of BPH. Data are presented as mean values + s.e.m., n = 10 biological replicates. Asterisks in (d,e) indicate significant differences in ko-lrr2 line compared with WT plants evaluated by two-sided Student’s t-test (**P < 0.01 and ***P < 0.001). f) Mature grain of ko-lrr2 and WT rice plants in the pest-controlled field. Bars, 1 cm. g−i) The 10-grain length (g) and 10-grain width (h), and 1,000-grain weight (i) of ko-lrr2 and WT rice lines in the pest-controlled field. Data are presented as mean values + s.e.m., n = 15 biological replicates. Asterisks in (g−i) indicate significant differences in ko-lrr2 lines compared with WT (XS110) plants evaluated by Bayesian analysis of variance (*P < 0.05, **P < 0.01, and ***P < 0.001). For P values, see source data. Experiments were repeated twice with similar results.

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Kuai, P., Lin, N., Ye, M. et al. Identification and knockout of a herbivore susceptibility gene enhances planthopper resistance and increases rice yield. Nat Food (2024). https://doi.org/10.1038/s43016-024-01044-4

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