Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Pi5 and Pii Paired NLRs Are Functionally Exchangeable and Confer Similar Disease Resistance Specificity

  • Vo, Kieu Thi Xuan (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Lee, Sang-Kyu (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Halane, Morgan K. (Department of Life Sciences, Pohang University of Science and Technology) ;
  • Song, Min-Young (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Hoang, Trung Viet (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Kim, Chi-Yeol (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Park, Sook-Young (Department of Plant Medicine, Sunchon National University) ;
  • Jeon, Junhyun (Department of Biotechnology, Yeungnam University) ;
  • Kim, Sun Tae (Department of Plant Bioscience, Pusan National University) ;
  • Sohn, Kee Hoon (Department of Life Sciences, Pohang University of Science and Technology) ;
  • Jeon, Jong-Seong (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University)
  • Received : 2019.04.09
  • Accepted : 2019.08.06
  • Published : 2019.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Effector-triggered immunity (ETI) is an effective layer of plant defense initiated upon recognition of avirulence (Avr) effectors from pathogens by cognate plant disease resistance (R) proteins. In rice, a large number of R genes have been characterized from various cultivars and have greatly contributed to breeding programs to improve resistance against the rice blast pathogen Magnaporthe oryzae. The extreme diversity of R gene repertoires is thought to be a result of co-evolutionary history between rice and its pathogens including M. oryzae. Here we show that Pii is an allele of Pi5 by DNA sequence characterization and complementation analysis. Pii-1 and Pii-2 cDNAs were cloned by reverse transcription polymerase chain reaction from the Pii-carrying cultivar Fujisaka5. The complementation test in susceptible rice cultivar Dongjin demonstrated that the rice blast resistance mediated by Pii, similar to Pi5, requires the presence of two nucleotide-binding leucine-rich repeat genes, Pii-1 and Pii-2. Consistent with our hypothesis that Pi5 and Pii are functionally indistinguishable, the replacement of Pii-1 by Pi5-1 and Pii-2 by Pi5-2, respectively, does not change the level of disease resistance to M. oryzae carrying AVR-Pii. Surprisingly, Exo70F3, required for Pii-mediated resistance, is dispensable for Pi5-mediated resistance. Based on our results, despite similarities observed between Pi5 and Pii, we hypothesize that Pi5 and Pii pairs require partially distinct mechanisms to function.

Keywords

References

  1. Bryan, G.T., Wu, K.S., Farrall, L., Jia, Y., Hershey, H.P., McAdams, S.A., Faulk, K.N., Donaldson, G.K., Tarchini, R., and Valent, B. (2000). A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12, 2033-2046. https://doi.org/10.2307/3871103
  2. Cesari, S., Kanzaki, H., Fujiwara, T., Bernoux, M., Chalvon, V., Kawano, Y., Shimamoto, K., Dodds, P., Terauchi, R., and Kroj, T. (2014). The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J. 33, 1941-1959. https://doi.org/10.15252/embj.201487923
  3. Chisholm, S.T., Coaker, G., Day, B., and Staskawicz, B.J. (2006). Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814. https://doi.org/10.1016/j.cell.2006.02.008
  4. Cui, H., Tsuda, K., and Parker, J.E. (2015). Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66, 487-511. https://doi.org/10.1146/annurev-arplant-050213-040012
  5. Deng, Y., Zhai, K., Xie, Z., Yang, D., Zhu, X., Liu, J., Wang, X., Qin, P., Yang, Y., Zhang, G., et al. (2017). Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355, 962-965. https://doi.org/10.1126/science.aai8898
  6. Ebron, L.A., Fukuta, Y., Imbe, T., Kato, H., Yanoria, J.M.T., Tsunematsu, H., Khush, G.S., and Yokoo, M. (2004). Estimation of genes in blast resistance in elite indica-type rice (Oryza sativa L.) varieties-bred at the international rice research institute. Breed. Sci. 54, 381-387. https://doi.org/10.1270/jsbbs.54.381
  7. Fujisaki, K., Abe, Y., Ito, A., Saitoh, H., Yoshida, K., Kanzaki, H., Kanzaki, E., Utsushi, H., Yamashita, T., Kamoun, S., et al. (2015). Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity. Plant J. 83, 875-887. https://doi.org/10.1111/tpj.12934
  8. Fuse, T., Sasaki, T., and Yano, M. (2001). Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol. 18, 219-222. https://doi.org/10.5511/plantbiotechnology.18.219
  9. Heidrich, K., Tsuda, K., Blanvillain-Baufume, S., Wirthmueller, L., Bautor, J., and Parker, J.E. (2013). Arabidopsis TNL-WRKY domain receptor RRS1 contributes to temperature-conditioned RPS4 auto-immunity. Front. Plant Sci. 4, 1-3.
  10. Huang, J., Si, W., Deng, Q., Li, P., and Yang, S. (2014). Rapid evolution of avirulence genes in rice blast fungus Magnaporthe oryzae. BMC Genet. 15, 45. https://doi.org/10.1186/1471-2156-15-45
  11. Inukai, T., Zeigler, R.S., Sarkarung, S., Bronson, M., Dung, L.V, Kinoshita, T., and Nelson, R.J. (1996). Development of pre-isogenic lines for rice blast-resistance by marker-aided selection from a recombinant inbred population. Theor. Appl. Genet. 93, 560-567. https://doi.org/10.1007/BF00417948
  12. Jacob, F., Vernaldi, S., and Maekawa, T. (2013). Evolution and conservation of plant NLR functions. Front. Immunol. 4, 1-16. https://doi.org/10.3389/fimmu.2013.00001
  13. Jeon, J.S., Chen, D., Yi, G.H., Wang, G.L., and Ronald, P.C. (2003). Genetic and physical mapping of Pi5(t), a locus associated with broad-spectrum resistance to rice blast. Mol. Genet. Genomics 269, 280-289. https://doi.org/10.1007/s00438-003-0834-2
  14. Jeon, J.S., Lee, S., Jung, K.H., Jun, S.H., Jeong, D.H., Lee, J., Kim, C., Jang, S., Lee, S., Yang, K., et al. (2000). T-DNA insertional mutagenesis for functional genomics in rice. Plant J. 22, 561-570. https://doi.org/10.1046/j.1365-313x.2000.00767.x
  15. Jia, Y., McAdams, S.A., Bryan, G.T., Hershey, H.P., and Valent, B. (2000). Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 4004-4014. https://doi.org/10.1093/emboj/19.15.4004
  16. Jia, Y. and Liu, G. (2011). Mapping quantitative trait loci for resistance to rice blast. Phytopathology 101, 176-181. https://doi.org/10.1094/PHYTO-06-10-0151
  17. Jones, J.D.G. and Dangl, J.L. (2006). The plant immune system. Nature 444, 323-329. https://doi.org/10.1038/nature05286
  18. Kang, H., Wang, Y., Peng, S., Zhang, Y., Xiao, Y., Wang, D., Qu, S., Li, Z., Yan, S., and Wang, Z. (2016). Dissection of the genetic architecture of rice resistance to the blast fungus Magnaporthe oryzae. Mol. Plant Pathol. 17, 959-972. https://doi.org/10.1111/mpp.12340
  19. Kanzaki, H., Nirasawa, S., Saitoh, H., Ito, M., Nishihara, M., Terauchi, R., and Nakamura, I. (2002). Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor. Appl. Genet. 105, 809-814. https://doi.org/10.1007/s00122-001-0817-9
  20. Kobayashi, N., Yanoria-Telebanco, M.J., Tsunematsu, H., Kato, H., IMBE, T., and Fukuta, Y. (2007). Development of new sets of international standard differential varieties for blast resistance in rice (Oryza sativa L.). Japan Agric. Res. Quart. 41, 31-37. https://doi.org/10.6090/jarq.41.31
  21. Lee, S.K., Song, M.Y., Seo, Y.S., Kim, H.K., Ko, S., Cao, P.J., Suh, J.P., Yi, G., Roh, J.H., Lee, S., et al. (2009). Rice Pi5-mediated resistance to Magnaporthe oryzae requires the presence of two coiled-coil-nucleotide-binding-leucine-rich repeat genes. Genetics 181, 1627-1638. https://doi.org/10.1534/genetics.108.099226
  22. Lu, L., Wang, Q., Jia, Y., Bi, Y.Q., Li, C.Y., Fan, H.C., and Li, J.B. (2019). Selection and mutation of the avirulence gene AVR-Pii of the rice blast fungus Magnaporthe oryzae. Plant Pathol. 2, 1-8. https://doi.org/10.1111/j.1365-3059.1953.tb00623.x
  23. Mackill, D.J. (1992). Inheritance of blast resistance in near-isogenic lines of rice. Phytopathology 82, 746-749. https://doi.org/10.1094/Phyto-82-746
  24. Maekawa, T., Kufer, T.A., and Schulze-Lefert, P. (2011). NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12, 817-826. https://doi.org/10.1038/ni.2083
  25. McDonald, B.A. and Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40, 349-379. https://doi.org/10.1146/annurev.phyto.40.120501.101443
  26. Miao, J., Guo, D., Zhang, J., Huang, Q., Qin, G., Zhang, X., Wan, J., Gu, H., and Qu, L.J. (2013). Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res. 23, 1233-1236. https://doi.org/10.1038/cr.2013.123
  27. Miki, D. and Shimamoto, K. (2004). Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 45, 490-495. https://doi.org/10.1093/pcp/pch048
  28. Munson, M. and Novick, P. (2006). The exocyst defrocked, a framework of rods revealed. Nat. Struct. Mol. Biol. 13, 577-581. https://doi.org/10.1038/nsmb1097
  29. Nakagawa, T., Suzuki, T., Murata, S., Nakamura, S., Hino, T., Maeo, K., Tabata, R., Kawai, T., Tanaka, K., Niwa, Y., et al. (2007). Improved gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095-2100. https://doi.org/10.1271/bbb.70216
  30. Nishimura, M.T., Monteiro, F., and Dangl, J.L. (2015). Treasure your exceptions: unusual domains in immune receptors reveal host virulence targets. Cell 161, 957-960. https://doi.org/10.1016/j.cell.2015.05.017
  31. Park, C.H., Shirsekar, G., Bellizzi, M., Chen, S., Songkumarn, P., Xie, X., Shi, X., Ning, Y., Zhou, B., Suttiviriya, P., et al. (2016). The E3 ligase APIP10 connects the effector AvrPiz-t to the NLR receptor Piz-t in rice. PLoS Pathog. 12, e1005529. https://doi.org/10.1371/journal.ppat.1005529
  32. Ray, S.K., Macoy, D.M., Kim, W.Y., Lee, S.Y., and Kim, M.G. (2019). Role of RIN4 in regulating PAMP-triggered immunity and effector-triggered immunity: current status and future perspectives. Mol. Cells 42, 503-511. https://doi.org/10.14348/molcells.2019.2433
  33. Satoh, Y., Miki, S., Ose, T., Oikawa, A., Maenaka, K., Terauchi, R., Asano, K. and Sone, T. (2014). Heterologous production, purification, and immunodetection of Magnaporthe oryzae avirulence protein AVR-Pia. Biosci. Biotechnol. Biochem. 78, 680-686. https://doi.org/10.1080/09168451.2014.893186
  34. Schulze-Lefert, P. and Panstruga, R. (2011). A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 16, 117-125. https://doi.org/10.1016/j.tplants.2011.01.001
  35. Selisana, S.M., Yanoria, M.J., Quime, B., Chaipanya, C., Lu, G., Opulencia, R., Wang, G.L., Mitchell, T., Correll, J., and Talbot, N.J. (2017). Avirulence (AVR) gene-based diagnosis complements existing pathogen surveillance tools for effective deployment of resistance (R) genes against rice blast disease. Phytopathology 107, 711-720. https://doi.org/10.1094/PHYTO-12-16-0451-R
  36. Singh, A.K., Singh, P.K., Arya, M., Singh, N.K., and Singh, U.S. (2015). Molecular screening of blast resistance genes in Rice using SSR markers. Plant Pathol. J. 31, 12-24. https://doi.org/10.5423/PPJ.OA.06.2014.0054
  37. Takagi, H., Uemura, A., Yaegashi, H., Tamiru, M., Abe, A., Mitsuoka, C., Utsushi, H., Natsume, S., Kanzaki, H., Matsumura, H., et al. (2013). MutMap-Gap: whole-genome resequencing of mutant F2 progeny bulk combined with de novo assembly of gap regions identifies the rice blast resistance gene Pii. New Phytol. 200, 276-283. https://doi.org/10.1111/nph.12369
  38. Tsunematsu, H., Yanoria, M.J.T., Ebron, L.A., Hayashi, N., Ando, I., Kato, H., Imbe, T., and Khush, G.S. (2000). Development of monogenic lines of rice for blast resistance. Breed. Sci. 50, 229-234. https://doi.org/10.1270/jsbbs.50.229
  39. Wang, X., Lee, S., Wang, J., Ma, J., Bianco, T., and Jia, Y. (2014). Current advances on genetic resistance to rice blast disease. In Rice: Germplasm, Genetics and Improvement, Y. Wengui, ed. (London, United Kingdom: IntechOpen), pp. 195-217.
  40. Wang, Y., Zhao, J.M., Zhang, L.X., Wang, P., Wang, S.W., Wang, H., Wang, X.X., Liu, Z.H., Zheng, W.J. (2016). Analysis of the diversity and function of the alleles of the rice blast resistance genes Piz-t, Pita and Pik in 24 rice cultivars. J. Integr. Agric. 15, 1423-1431. https://doi.org/10.1016/S2095-3119(15)61207-2
  41. Wu, C., Bordeos, A., Madamba, M.R.S., Baraoidan, M., Ramos, M., Wang, G.L., Leach, J.E., and Leung, H. (2008). Rice lesion mimic mutants with enhanced resistance to diseases. Mol. Genet. Genomics 279, 605-619. https://doi.org/10.1007/s00438-008-0337-2
  42. Wu, K., Xu, T., Guo, C., Zhang, X., and Yang, S. (2012). Heterogeneous evolutionary rates of Pi2 / 9 homologs in rice. BMC Genet. 13, 73.
  43. Wu, L., Chen, H., Curtis, C., and Fu, Z.Q. (2014). Go in for the kill: How plants deploy effector-triggered immunity to combat pathogens. Virulence 5, 710-721. https://doi.org/10.4161/viru.29755
  44. Yi, G., Lee, S.K., Hong, Y.K., Cho, Y.C., Nam, M.H., Kim, S.C., Han, S.S., Wang, G.L., Hahn, T.R., Ronald, P.C., et al. (2004). Use of Pi5(t) markers in markerassisted selection to screen for cultivars with resistance to Magnaporthe grisea. Theor. Appl. Genet. 109, 978-985. https://doi.org/10.1007/s00122-004-1707-8
  45. Yoshida, K., Saitoh, H., Fujisawa, S., Kanzaki, H., Matsumura, H., Yoshida, K., Tosa, Y., Chuma, I., Takano, Y., Win, J., et al. (2009). Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21, 1573-1591. https://doi.org/10.1105/tpc.109.066324
  46. Zhang, Y., Lubberstedt, T., and Xu, M. (2013). The genetic and molecular basis of plant resistance to pathogens. J. Genet. Genomics 40, 23-35. https://doi.org/10.1016/j.jgg.2012.11.003

Cited by

  1. Integrated Strategies for Durable Rice Blast Resistance in Sub-Saharan Africa vol.105, pp.10, 2019, https://doi.org/10.1094/pdis-03-21-0593-fe