Abstract
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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.
Abstract
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.
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References
Bonman JM (1992) Durable resistance to rice blast disease-environmental influences. Euphytica 63:115–123
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 61:251–259
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 325:998–1001
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 4:4550
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 137–147
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 64:498–510
Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3:824–834
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 110:9577–9582
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 10:36
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 93:560–567
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 21:260–268
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 47:351–358
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 170:114–126
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 6:605–620
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 7:10362
Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932
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 9:199–207
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 19:1127–1137
Midoh N, Iwata M (1996) Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol 37:9–18
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 279:415–427
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 86:1071–1075
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:e6
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 182:1303–1311
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 19:2064–2076
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 10:175
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 59:253–260
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:RESEARCH0034
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 136:1421–1434
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 28:999–1007
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 169:2277–2293
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:e93275
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)
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 84:20–28
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This work was supported by JSPS KAKENHI Grant No. JP16K07549.
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Communicated by Mingliang Xu.
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Inukai, T., Nagashima, S. & Kato, M. Pid3-I1 is a race-specific partial-resistance allele at the Pid3 blast resistance locus in rice. Theor Appl Genet 132, 395–404 (2019). https://doi.org/10.1007/s00122-018-3227-y
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DOI: https://doi.org/10.1007/s00122-018-3227-y