Theoretical and Applied Genetics

, Volume 132, Issue 2, pp 395–404 | Cite as

Pid3-I1 is a race-specific partial-resistance allele at the Pid3 blast resistance locus in rice

  • Tsuyoshi InukaiEmail author
  • Saki Nagashima
  • Miyako Kato
Original Article


Key message

The rice blast resistance QTL detected on chromosome 6 in MC276 is Pid3-I1, one of the multiple alleles at the Pid3 locus. Pid3-I1 shows race-specific partial resistance.


Many of the quantitative trait loci (QTLs) for rice blast resistance reported to date remain unidentified. In the present study, we focused on qBRM6.2, a known blast-resistance QTL in experimental resistant rice line MC276. A CO39 near-isogenic line (NIL) carrying qBRM6.2 from MC276 was developed here, and we showed that qBRM6.2 resistance was partial but race specific to Japanese blast isolates using the NIL. Because defense genes in the NIL were expressed sooner than those in CO39 after inoculation with a blast isolate, qBRM6.2 resistance appeared to be an induced resistance. Next, we demonstrated that qBRM6.2 was located within a 123-kb interval on chromosome 6. Among the six genes annotated in the interval, only four genes appeared to be functional. Among these four, a polymorphism between CO39 and the NIL for qBRM6.2 at the amino acid sequence level was detected only in Os06g0330400 that encodes a fatty acid hydroxylase domain-containing protein and in Os06g0330100, the blast resistance locus Pid3, that encodes a nucleotide-binding site–leucine-rich repeat protein. Moreover, the allele at the Pid3 locus in the NIL was Pid3-I1, originally identified as a complete blast resistance gene in Kasalath. To clarify whether Pid3-I1 is qBRM6.2, we investigated the resistance phenotype of Pid3-I1 to Japanese isolates using Nipponbare transgenic lines that express Pid3-I1. The results showed that Pid3-I1 was a race-specific but partial-resistance allele at the Pid3 locus, suggesting strongly that Pid3-I1 is qBRM6.2. The discrepancy in the phenotype of Pid3-I1 between the present and previous reports is also discussed.



This work was supported by JSPS KAKENHI Grant No. JP16K07549.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2018_3227_MOESM1_ESM.pdf (17.7 mb)
Supplementary material 1 (PDF 18118 kb)


  1. Bonman JM (1992) Durable resistance to rice blast disease-environmental influences. Euphytica 63:115–123CrossRefGoogle Scholar
  2. Ebitani T, Hayashi N, Omoteno M, Ozaki H, Yano M, Morikawa M, Fukuta Y (2011) Characterization of Pi13, a blast resistance gene that maps to chromosome 6 in indica rice. (Oryza sativa L. variety, Kasalath). Breed Sci 61:251–259CrossRefGoogle Scholar
  3. Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001CrossRefGoogle Scholar
  4. Fukuoka S, Yamamoto S, Mizobuchi R, Yamanouchi U, Ono K, Kitazawa N, Yasuda N, Fujita Y, Nguyen TTT, Koizumi S, Sugimoto K, Matsumoto T, Yano M (2014) Multiple functional polymorphisms in a single disease resistance gene in rice enhance durable resistance to blast. Sci Rep 4:4550CrossRefGoogle Scholar
  5. Harwood WA, Bartlett JG, Alves SC, Perry M, Smedley MA, Leyland N, Snape JW (2009) Barley transformation using agrobacterium-mediated techniques. In: Jones HD, Shewry PR (eds) Methods in molecular biology, transgenic wheat, barley and oats, vol 478. Humana Press, Totowa, pp 137–147CrossRefGoogle Scholar
  6. Hayashi N, Inoue H, Kato T, Funao T, Shirota M, Shimizu T, Kanamori H, Yamane H, Hayano-Saito Y, Matsumoto T, Yano M, Takatsuji H (2010) Durable panicle blast-resistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. Plant J 64:498–510CrossRefGoogle Scholar
  7. Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3:824–834CrossRefGoogle Scholar
  8. Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A, Sugano S, Jiang CJ, Takatsuji H (2013) Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc Natl Acad Sci USA 110:9577–9582CrossRefGoogle Scholar
  9. Inoue H, Nakamura M, Mizubayashi T, Takahashi A, Sugano S, Fukuoka S, Hayashi N (2017) Panicle blast 1 (Pb1) resistance is dependent on at least four QTLs in the rice genome. Rice 10:36CrossRefGoogle Scholar
  10. Inukai T, Zeigler RS, Sarkarung S, Bronson M, Dung LV, Kinoshita T, Nelson RJ (1996) Development of pre-isogenic lines for rice blast resistance by marker-aided selection from a recombinant inbred population. Theor Appl Genet 93:560–567CrossRefGoogle Scholar
  11. Kim B, Masuta C, Matsuura H, Takahashi H, Inukai T (2008) Veinal necrosis induced by turnip mosaic virus infection in Arabidopsis is a form of defense response accompanying HR-like cell death. Mol Plant Microbe Interact 21:260–268CrossRefGoogle Scholar
  12. Li QF, Zhang GY, Dong ZW, Yu HX, Gu MH, Sun SS, Liu QQ (2009) Characterization of expression of the OsPUL gene encoding a pullulanase-type debranching enzyme during seed development and germination in rice. Plant Physiol Biochem 47:351–358CrossRefGoogle Scholar
  13. Li W, Zhu Z, Chern M, Yin J, Yang C, Ran L, Cheng M, He M, Wang K, Wang J, Zhou X, Zhu X, Chen Z, Wang J, Zhao W, Ma B, Qin P, Chen W, Wang Y, Liu J, Wang W, Wu X, Li P, Wang J, Zhu L, Li S, Chen X (2017) A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170:114–126CrossRefGoogle Scholar
  14. Liu W, Liu J, Ning Y, Ding B, Wang X, Wang Z, Wang GL (2013) Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol Plant 6:605–620CrossRefGoogle Scholar
  15. Lv Q, Huang Z, Xu X, Tang L, Liu H, Wang C, Zhou Z, Xin Y, Xing J, Peng Z, Li X, Zheng T, Zhu L (2017) Allelic variation of the rice blast resistance gene Pid3 in cultivated rice worldwide. Sci Rep 7:10362CrossRefGoogle Scholar
  16. Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932CrossRefGoogle Scholar
  17. McCouch SR, Teytelman L, Xu Y, Lobos KB, Clare K, Walton M, Fu B, Maghirang R, Li Z, Xing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199–207CrossRefGoogle Scholar
  18. Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant Microbe Interact 19:1127–1137CrossRefGoogle Scholar
  19. Midoh N, Iwata M (1996) Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol 37:9–18CrossRefGoogle Scholar
  20. Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics 279:415–427CrossRefGoogle Scholar
  21. Pan Q, Wang L, Ikehashi H, Tanisaka T (1996) Identification of a new blast resistance gene in the indica rice cultivar Kasalath using Japanese differential cultivars and isozyme markers. Phytopathology 86:1071–1075CrossRefGoogle Scholar
  22. Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang CC, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6CrossRefGoogle Scholar
  23. Shang J, Tao Y, Chen X, Zou Y, Lei C, Wang J, Li X, Zhao X, Zhang M, Lu Z, Xu J, Cheng Z, Wan J, Zhu L (2009) Identification of a new rice blast resistance gene, Pid3, by genomewide comparison of paired nucleotide-binding site–leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics 182:1303–1311CrossRefGoogle Scholar
  24. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19:2064–2076CrossRefGoogle Scholar
  25. Takahashi A, Hayashi N, Miyao A, Hirochika H (2010) Unique features of the rice blast resistance Pish locus revealed by large scale retrotransposon-tagging. BMC Plant Biol 10:175CrossRefGoogle Scholar
  26. Takehisa H, Yasuda M, Fukuta Y, Kobayashi N, Hayashi N, Nakashita H, Abe T, Sato T (2009) Genetic analysis of resistance genes in an Indica-type rice (Oryza sativa L.) Kasalath using DNA markers. Breed Sci 59:253–260CrossRefGoogle Scholar
  27. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034CrossRefGoogle Scholar
  28. Wang GL, Mackill DJ, Bonman JM, McCouch SR, Champoux MC, Nelson RJ (1994) RFLP mapping of genes conferring complete and partial resistance to blast in a durably resistant rice cultivar. Genetics 136:1421–1434Google Scholar
  29. Wang D, Qin Y, Han J, Zhang L, Xu X, Liu X, Wang C, Liu X (2014) Expression analysis of innate immunity related genes in the true/field blast resistance gene-mediated defense response. Biotechnol Biotechnol Equip 28:999–1007CrossRefGoogle Scholar
  30. Wisser RJ, Sun Q, Hulbert SH, Kresovich S, Nelson RJ (2005) Identification and characterization of regions of the rice genome associated with broad-spectrum, quantitative disease resistance. Genetics 169:2277–2293CrossRefGoogle Scholar
  31. Xu X, Lv Q, Shang J, Pang Z, Zhou Z, Wang J, Jiang G, Tao Y, Xu Q, Lim X, Zhao X, Li S, Xu J, Zhu L (2014) Excavation of Pid3 orthologs with differential resistance spectra to Magnaporthe oryzae in rice resource. PLoS ONE 9:e93275CrossRefGoogle Scholar
  32. Yamasaki Y, Kiyosawa S (1966) Studies on inheritance of resistance of rice varieties to blast, 1. Inheritance of resistance of Japanese varieties to several strains of the fungus. Bull Natl Inst Agric Sci D14:39–69 (in Japanese) Google Scholar
  33. Zhang X, Yang S, Wang J, Jia Y, Huang J, Tan S, Zhong Y, Wang L, Gu L, Chen JQ, Pan Q, Bergelson J, Tian D (2015) A genome-wide survey reveals abundant rice blast R genes in resistant cultivars. Plant J 84:20–28CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Research Faculty of AgricultureHokkaido UniversitySapporoJapan

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