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Resistance of rice to insect pests mediated by suppression of serotonin biosynthesis

Nature Plants volume 4, pages 338–344 (2018)Cite this article

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Abstract

Rice is one of the world’s most important foods, but its production suffers from insect pests, causing losses of billions of dollars, and extensive use of environmentally damaging pesticides for their control1,2. However, the molecular mechanisms of insect resistance remain elusive. Although a few resistance genes for planthopper have been cloned, no rice germplasm is resistant to stem borers. Here, we report that biosynthesis of serotonin, a neurotransmitter in mammals3, is induced by insect infestation in rice, and its suppression confers resistance to planthoppers and stem borers, the two most destructive pests of rice2. Serotonin and salicylic acid derive from chorismate4. In rice, the cytochrome P450 gene CYP71A1 encodes tryptamine 5-hydroxylase, which catalyses conversion of tryptamine to serotonin5. In susceptible wild-type rice, planthopper feeding induces biosynthesis of serotonin and salicylic acid, whereas in mutants with an inactivated CYP71A1 gene, no serotonin is produced, salicylic acid levels are higher and plants are more insect resistant. The addition of serotonin to the resistant rice mutant and other brown planthopper-resistant genotypes results in a loss of insect resistance. Similarly, serotonin supplementation in artificial diet enhances the performance of both insects. These insights demonstrate that regulation of serotonin biosynthesis plays an important role in defence, and may prove valuable for breeding insect-resistant cultivars of rice and other cereal crops.

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Fig. 1: Mutation in CYP71A1 resulting in the suppression of serotonin synthesis confers resistance to BPH.
Fig. 2: Addition of exogenous serotonin abolishes BPH resistance in rice.
Fig. 3: BPH infestation induces biosynthesis of salicylic acid, but salicylic acid and serotonin suppress each other, suggesting mutual negative feedback.
Fig. 4: SSB infestation induces expression of CYP71A1 but mutation in this gene enhances resistance to SSB.

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Acknowledgements

This study was supported by grants from National Key Research and Development Programme of China (2016YFD0102103), Agro-scientific Research in the Public Interest (201403030), Zhejiang Provincial S & T Project on Breeding of Agricultural (Food) Crops (2016C02050-2), China Postdoctoral Research Project (2017M620248), Dabeinong Funds for Discipline Development and Talent Training in Zhejiang University, China National Key Laboratory of Rice Biology, and the 111 Project. Assistance for melatonin measurement from J. Yu’s group is appreciated. We are grateful to T. Mou and Q. Fu for provision of BPH-resistant genotypes.

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  1. These authors contributed equally: Hai-ping Lu, Ting Luo, Hao-wei Fu.

Authors and Affiliations

  1. State Key Laboratory of Rice Biology, Zhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, Hangzhou, China

    Hai-ping Lu, Yuan-yuan Tan, Jian-zhong Huang & Qing-yao Shu

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

    Ting Luo, Long Wang, Gong-yin Ye & Yong-gen Lou

  3. Jiaxing Academy of Agricultural Sciences, Zhejiang, China

    Hao-wei Fu

  4. Wuxi Hupper Bioseed Ltd., Wuxi, Jiangsu, China

    Qing Wang

  5. School of Biology, Newcastle University, Newcastle upon Tyne, UK

    Angharad M. R. Gatehouse

  6. Hubei Collaborative Innovation Center for Grain Industry, Jingzhou, Hubei, China

    Qing-yao Shu

Authors
  1. Hai-ping Lu
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Contributions

Q.Y.S., Y.G.L., A.M.R.G., G.Y.Y. and J.Z.H. contributed to study design and data analysis, H.L. contributed to overall study and data analysis, T.L. contributed to BPH and WBPH resistance studies, H.W.F. contributed to Jiazhe LM mutant development and field studies, L.W. contributed SSB resistance studies, Q.W. and Y.Y.T. contributed to the development and characterization of knockout mutants, and A.M.R.G. and Q.Y.S. wrote the manuscript. All authors read and approve the paper.

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Correspondence to Angharad M. R. Gatehouse, Yong-gen Lou or Qing-yao Shu.

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Supplementary Information

Supplementary Figures 1–12, Supplementary Tables 1–2, Supplementary Procedures, Supplementary References and precise P values.

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Lu, Hp., Luo, T., Fu, Hw. et al. Resistance of rice to insect pests mediated by suppression of serotonin biosynthesis. Nature Plants 4, 338–344 (2018). https://doi.org/10.1038/s41477-018-0152-7

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