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Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice

Nature Genetics volume 50, pages 297–306 (2018)Cite this article

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Abstract

The brown planthopper (BPH) and white-backed planthopper (WBPH) are the most destructive insect pests of rice, and they pose serious threats to rice production throughout Asia. Thus, there are urgent needs to identify resistance-conferring genes and to breed planthopper-resistant rice varieties. Here we report the map-based cloning and functional analysis of Bph6, a gene that confers resistance to planthoppers in rice. Bph6 encodes a previously uncharacterized protein that localizes to exocysts and interacts with the exocyst subunit OsEXO70E1. Bph6 expression increases exocytosis and participates in cell wall maintenance and reinforcement. A coordinated cytokinin, salicylic acid and jasmonic acid signaling pathway is activated in Bph6-carrying plants, which display broad resistance to all tested BPH biotypes and to WBPH without sacrificing yield, as these plants were found to maintain a high level of performance in a field that was heavily infested with BPH. Our results suggest that a superior resistance gene that evolved long ago in a region where planthoppers are found year round could be very valuable for controlling agricultural insect pests.

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Fig. 1: Map-based cloning of Bph6.
Fig. 2: Molecular characterization of Bph6.
Fig. 3: Demonstration that BPH6 interacts with exocyst subunit OsEXO70E1.
Fig. 4: Characterization of exocyst gene expression and cell walls in 9311-Bph6-NIL and 9311 plants.
Fig. 5: Analyses of phytohormones in Bph6-carrying plants.
Fig. 6: Characterization of Bph6-mediated resistance.
Fig. 7: Evolution of Bph6 alleles in rice.

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Acknowledgements

We thank Q. Qian (China National Rice Research Institute), L. Han (Chinese Academy of Agricultural Sciences), L. Yan (Jiangxi Academy of Agricultural Sciences) and D. Pan (Guangdong Academy of Agricultural Sciences) for kindly providing rice germplasm, S. Wang (Huazhong Agricultural University) for kindly providing the rice disease pathogen PXO145, Y. Lin (Huazhong Agricultural University) for kindly providing the striped stem borer insects, D. Zeng (China National Rice Research Institute) for kindly providing the WBPH insects, Y. Liu for suggestions for the experiments, and Q. Zhang, R. He and J. Blackwell for edits and suggestions. This work was supported by grants from the National Natural Science Foundation of China (31230060 and 31630063, both to G.H.), the National Program on Research and Development of Transgenic Plants (2016ZX08009-003-001 to G.H.) and the National Key Research and Development Program (2016YFD0100600 and 2016YFD0100900, both to G.H.).

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  1. Jianping Guo, Chunxue Xu and Di Wu contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, China

    Jianping Guo, Chunxue Xu, Di Wu, Yan Zhao, Yongfu Qiu, Xiaoxiao Wang, Shengli Jing, Xinxin Shangguan, Huiying Wang, Yinhua Ma, Liang Hu, Yan Wu, Shaojie Shi, Wenliang Wang, Lili Zhu, Rongzhi Chen, Bo Du & Guangcun He

  2. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

    Yidan Ouyang

  3. Key Laboratory of Analytical Chemistry for Biology and Medicine (Ministry of Education), College of Chemistry and Molecular Sciences, Wuhan University, Wuhan, China

    Baodong Cai & Yuqi Feng

  4. BGI-Shenzhen, Shenzhen, China

    Xin Liu & Xun Xu

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  1. Jianping Guo
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Contributions

G.H. conceived and supervised the project; G.H. and J.G. designed the experiments; J.G. performed most of the experiments; C.X., Y.Z., D.W., B.D., X.W., Y.O., X.L., W.W., Y.Q., S.J., B.C., X.S., H.W., Y.M., Y.W., L.H., S.S., L.Z., X.X., R.C. and Y.F. performed some of the experiments; and J.G., C.X., D.W., B.D., Y.Z. and G.H. analyzed data and wrote the manuscript.

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Correspondence to Bo Du or Guangcun He.

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Supplementary Text and Figures

Supplementary Figures 1–27 and Supplementary Tables 1, 2, 4, 5, 7, 10 and 11

Life Sciences Reporting Summary

Supplementary Table 3

GeneChip data for comparing Nip-Bph6-NIL and Bph6-RNAi plants

Supplementary Table 6

Information on accessions of wild rice and cultivated varieties that were sequenced in the Bph6 coding region

Supplementary Table 8

List of SNPs between Swarnalata or Nipponbare and the 80 haplotypes

Supplementary Table 9

List of indels between Swarnalata or Nipponbare and the 80 haplotypes

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Guo, J., Xu, C., Wu, D. et al. Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat Genet 50, 297–306 (2018). https://doi.org/10.1038/s41588-018-0039-6

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