Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice

Subjects

Abstract

The brown planthopper (BPH) is the most destructive pest of rice (Oryza sativa) and a substantial threat to rice production, causing losses of billions of dollars annually1,2. Breeding of resistant cultivars is currently hampered by the rapid breakdown of BPH resistance2. Thus, there is an urgent need to identify more effective BPH-resistance genes. Here, we report molecular cloning and characterization of Bph3, a locus in rice identified more than 30 years ago that confers resistance to BPH. We show that Bph3 is a cluster of three genes encoding plasma membrane–localized lectin receptor kinases (OsLecRK1-OsLecRK3). Introgression of Bph3 into susceptible rice varieties by transgenic or marker-assisted selection strategies significantly enhanced resistance to both the BPH and the white back planthopper. Our results suggest that these lectin receptor kinase genes function together to confer broad-spectrum and durable insect resistance and provide a resource for molecular breeding of insect-resistant rice cultivars.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Comparison of BPH resistance in Rathu Heenati (RH) and 02428.
Figure 2: Mapping of Bph3 and polymorphisms between resistant and susceptible varieties.
Figure 3: OsLecRK genes contribute additively to BPH resistance.
Figure 4: Origin of Bph3 and marker assisted selection-based breeding of BPH-resistant cultivars.

Similar content being viewed by others

Accession codes

Primary accessions

NCBI Reference Sequence

References

  1. Piper, R. Pests: a Guide to the World's Most Maligned, Yet Misunderstood Creatures (Greenwood Press, California, 2011).

  2. Cheng, X., Zhu, L. & He, G. The understanding of molecular interaction between rice and brown planthopper. Mol. Plant 6, 621–634 (2013).

    Article  CAS  Google Scholar 

  3. Nagata, T. Insecticide resistance in the brown planthopper. Chin. J. Entomol 4, 117–124 (1984).

    Google Scholar 

  4. Wu, H. et al. Fine mapping of brown planthopper (Nilaparvata lugens Stål) resistance gene Bph28(t) in rice (Oryza sativa L.). Mol. Breed. 33, 909–918 (2014).

    Article  CAS  Google Scholar 

  5. Lv, W. et al. BAC and RNA sequencing reveal the brown planthopper resistance gene BPH15 in a recombination cold spot that mediates a unique defense mechanism. BMC Genomics 15, 674 (2014).

    Article  Google Scholar 

  6. Du, B. et al. Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc. Natl. Acad. Sci. USA 106, 22163–22168 (2009).

    Article  CAS  Google Scholar 

  7. Tamura, Y. et al. Map-based cloning and characterization of a brown planthopper resistance gene BPH26 from Oryza sativa L. ssp. indica cultivar ADR52. Sci. Rep. 4, 5872 (2014).

    Article  Google Scholar 

  8. Cruz, P.A., Arida, A., Heong, K.L. & Horgan, F.G. Aspects of brown planthopper adaptation to resistant rice varieties with the Bph3 gene. Entomol. Exp. Appl. 141, 245–257 (2011).

    Article  CAS  Google Scholar 

  9. Laksminarayana, A. & Khush, G.S. New genes for resistance to the brown planthopper in rice. Crop Sci. 17, 96–100 (1977).

    Article  Google Scholar 

  10. Pathak, P.K. & Heinrichs, E.A. Selection of biotype 2 and 3 population of Nilaparvata lugens (Homoptera, Delphacidae) by exposure to resistant rice varieties. Environ. Entomol. 11, 85–90 (1982).

    Article  Google Scholar 

  11. Ghaffar, M.B., Pritchard, J. & Ford-Lloyd, B. Brown planthopper (Nilaparvata lugens Stål) feeding behaviour on rice germplasm as an indicator of resistance. PLoS ONE 6, e22137 (2011).

    Article  CAS  Google Scholar 

  12. Sun, L., Su, C., Wang, C., Zhai, H. & Wan, J. Mapping of a major resistance gene to the brown planthopper in the rice cultivar Rathu Heenati. Breed. Sci. 55, 391–396 (2005).

    Article  CAS  Google Scholar 

  13. Xiong, Z. et al. Comparative physical mapping of rice BAC clones linked to resistance genes Glh, Bph-3 and xa-5 in Oryza sativa L. and O. granulata Nees et Arn. ex Watt. Chin. Sci. Bull. 49, 591–596 (2004).

    Article  CAS  Google Scholar 

  14. Vaid, N., Pandey, P.K. & Tuteja, N. Genome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice. Plant Mol. Biol. 80, 365–388 (2012).

    Article  CAS  Google Scholar 

  15. Singh, P. & Zimmerli, L. Lectin receptor kinases in plant innate immunity. Front. Plant Sci. 4, 124 (2013).

    Article  Google Scholar 

  16. Gilardoni, P.A., Hettenhausen, C., Baldwin, I.T. & Bonaventure, G. Nicotiana attenuata LECTIN RECEPTOR KINASE1 suppresses the insect-mediated inhibition of induced defense responses during Manduca sexta herbivory. Plant Cell 23, 3512–3532 (2011).

    Article  CAS  Google Scholar 

  17. Chen, X. et al. A B-lectin receptor kinase gene conferring rice blast resistance. Plant J. 46, 794–804 (2006).

    Article  CAS  Google Scholar 

  18. Cheng, X. et al. A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J. 76, 687–698 (2013).

    Article  CAS  Google Scholar 

  19. Bharathi, M. & Chelliah, S. in Rice genetics II, Proceedings of the second international rice genetics Symposium (International Rice Research Institute, Philippines), 255–261 (2002).

  20. DellaPenna, D. & O'Connor, S.E. Plant gene clusters and opiates. Science 336, 1648–1649 (2012).

    Article  CAS  Google Scholar 

  21. Cook, D.E. et al. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338, 1206–1209 (2012).

    Article  CAS  Google Scholar 

  22. Wu, J.T., Heinrichs, E.A. & Medrana, F.G. Resistance of wild rice Oryza spp to the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Environ. Entomol. 15, 648–653 (1986).

    Article  Google Scholar 

  23. Xu, X. et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat. Biotechnol. 30, 105–111 (2012).

    Article  CAS  Google Scholar 

  24. Madurangi, S.A.P., Ratnasekera, D., Hemachandra, P.V. & Senanayake, S.G.J.N. in Proceedings of the 15th International Forestry and Environment Symposium. (eds. D. Ranasinghe, et al.). Department of Forestry and Environmental Science, University of Sri Jayewardenepura, Sri Lanka, 172–175 (2010).

  25. Shen, J., Wang, Y., Sogawa, K., Hattori, M. & Liu, G. Virulence of the populations of the whitebacked planthopper, So gat ella furcifera reared on different resistant rice varieties. Chin. J. Rice Sci. 11, 57–61 (2003).

    Google Scholar 

  26. Dodds, P.N. & Rathjen, J.P. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11, 539–548 (2010).

    Article  CAS  Google Scholar 

  27. Jones, J.D. & Dangl, J.L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  Google Scholar 

  28. Song, W.Y. et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21 . Science 270, 1804–1806 (1995).

    Article  CAS  Google Scholar 

  29. Naito, K. et al. Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol. Plant Microbe Interact. 21, 1165–1174 (2008).

    Article  CAS  Google Scholar 

  30. Lacombe, S. et al. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28, 365–369 (2010).

    Article  CAS  Google Scholar 

  31. Abramovitch, R.B., Anderson, J.C. & Martin, G.B. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 7, 601–611 (2006).

    Article  CAS  Google Scholar 

  32. Gouhier-Darimont, C., Schmiesing, A., Bonnet, C., Lassueur, S. & Reymond, P. Signalling of Arabidopsis thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity. J. Exp. Bot. 64, 665–674 (2013).

    Article  CAS  Google Scholar 

  33. Singh, P. et al. The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity. Plant Cell 24, 1256–1270 (2012).

    Article  CAS  Google Scholar 

  34. Kanzaki, H. et al. NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death. Planta 228, 977–987 (2008).

    Article  CAS  Google Scholar 

  35. Choi, J. et al. Identification of a plant receptor for extracellular ATP. Science 343, 290–294 (2014).

    Article  CAS  Google Scholar 

  36. Li, Q., Luo, S.Y., Shi, A.X., Wei, S.M. & Huang, F.K. The biotypes of brown planthopper [Nilaparvata lugens (Stål)] with a view to its control. Acta Entomol. Sin. 40, 139–146 (1997).

    Google Scholar 

  37. Chen, Y. et al. Geographical populations of brown planthopper in Nanning of South China and in Vietnam: a comparative study. Chin. J. Appl. Econ. 24, 190–196 (2013).

    Google Scholar 

  38. Heinrichs, E., Medrano, F. & Rapusas, H. Genetic Evaluation for Insect Resistance in Rice (International Rice Research Institute, Philippines, 1985).

  39. Pathak, P., Saxena, R. & Heinrichs, E. Parafilm sachet for measuring honeydew excretion by Nilaparvata lugens on rice. J. Econ. Entomol. 75, 194–195 (1982).

    Article  Google Scholar 

  40. Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271–282 (1994).

    Article  CAS  Google Scholar 

  41. Nelson, B., Cai, X. & Nebenfuhr, A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126–1136 (2007).

    Article  CAS  Google Scholar 

  42. Wang, G. & Valent, B. Advances in Genetics, Genomics and Control of Rice Blast Disease (Springer, 2009).

  43. Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741–745 (2005).

    Article  CAS  Google Scholar 

  44. Swofford, D. paup*. Phylogenetic Analysis Using Parsimony (* and other methods), version 4, beta 10. Sinauer Associates, Sunderland, MA. (1998).

  45. Belousov, V.V. et al. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3, 281–286 (2006).

    Article  CAS  Google Scholar 

  46. Gallagher, S.R. in GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression (ed. Gallagher, S.R.) 47–59 (San Diego: Academic Press, 1992).

Download references

Acknowledgements

This work was supported by Jiangsu 333 Program (BRA2012126), NSFC (31471470), 863 Program of China (2012AA101101, 2011AA10A101 and 2011BAD35B02-02), National Science and Technology Supporting Program (2011BAD35B02-02), National Key Transformation Program (2014ZX08001-001), Jiangsu Science and Technology Development Program (BE2012303, BK2010016), and the Jiangsu PAPD program. We thank R. Guan (Nanjing Agricultural University) and J. Wang (Chinese Academy of Agricultural Sciences) for statistical analysis, and J. Zhou (Chinese Academy of Sciences), W. Terzaghi (Wilkes University) and C. Lin (UC-LA) for proofreading the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

Y.Q.L., H.K., Z.S., G.P. and J.He performed genetic analysis and mapping of Bph3; X. Zhang, X.G. and L.J. performed the genetic transformation; H. Wu, H.C., Q.W. and F.Z. performed the construction of vectors; K.Z., Y.R. and Y.W. performed the subcellular localization; X. Zheng, Z.Z., Q.L. and F.W. performed sequence analysis; Y.L.L., J. Hu, L.C. and X.C. performed the phenotypic analysis. J.W., H. Wang and C.W. directed the project and wrote the manuscript.

Corresponding author

Correspondence to Jianmin Wan.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–11 and Supplementary Tables 1 and 2 (PDF 2267 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Wu, H., Chen, H. et al. A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nat Biotechnol 33, 301–305 (2015). https://doi.org/10.1038/nbt.3069

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt.3069

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing