Chin Bull Bot ›› 2019, Vol. 54 ›› Issue (2): 265-276.doi: 10.11983/CBB18194

;

• SPECIAL TOPICS • Previous Articles     Next Articles

Progress of Cloning and Breeding Application of Blast Resistance Genes in Rice and Avirulence Genes in Blast Fungi

Yang Dewei1,2,Wang Mo1,Han Libo1,Tang Dingzhong1,Li Shengping1,3,*()   

  1. 1 Plant Immunity Center, Fujian Agriculture and Forestry University, Fuzhou 350002, China
    2 Institute of Rice, Fujian Academy of Agricultural Sciences, Fuzhou 350018, China
    3 Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou 350002, China
  • Received:2018-09-12 Accepted:2019-01-08 Online:2019-09-01 Published:2019-03-01
  • Contact: Li Shengping E-mail:lishun1981@126.com

Abstract:

Rice blast, caused by Magnaporthe oryzae, is one of the most destructive diseases of rice worldwide. The identification and utilization of resistance genes are the basis and key factors for breeding resistance rice cultivars. With the availability of genomic sequences of both Oryza sativa and M. oryzae, rice has become one of the model systems for dissecting the molecular interactions between plants and pathogens. In this paper, we summarize the current status of genetics, mapping, cloning and breeding application of the genes resistant to blast. Using bioinformatics analysis, we analyzed the distribution of all NBS-LRR type of disease resistance genes on the 12 chromosomes of the rice genome and also preliminarily summarized the identified avirulence genes as well as interactions between the resistance proteins and the avirulence proteins. Finally, we analyzed and discussed the problems in rice breeding and prospects for research. This review will provide useful suggestions for further research on rice blast resistance breeding and disease resistance mechanisms.

Key words: rice blast, mapping, cloning, breeding application, avirulence genes

Table 1

Identified QTL of blast resistance and protein of NBS domain in rice"

染色体 1 2 3 4 5 6 7 8 9 10 11 12 总计
QTLs数量 34 22 8 16 3 18 19 8 10 1 16 28 183
抗性蛋白数量 45 33 18 31 20 35 27 47 23 31 154 59 523

Table 2

Cloned blast resistance genes in rice"

基因 染色体 供体 编码蛋白 参考文献
Pi37 1 St. No. 1 NBS-LRR Lin et al., 2007
Pish 1 日本晴 NBS-LRR Takahashi et al., 2010b
Pit 1 K59 NBS-LRR Hayashi et al., 2010
Pi35 1 Hokkai 188 NBS-LRR Fukuoka et al., 2014
Pi64 1 NBS-LRR Ma et al., 2015
Pib 2 IR24, BL1 NBS-LRR Wang et al., 1999
Bsrd-1 3 地谷 MYB转录因子 Li et al., 2017
pi-21 4 Owarihatamochi 富含脯氨酸蛋白 Fukuoka et al., 2009
Pi-63 4 Kahei NBS-LRR Xu et al., 2014
Pi2 6 Jefferson NBS-LRR Zhou et al., 2006
Pi9 6 75-1-127 NBS-LRR Qu et al., 2006
Piz-t 6 Zenith NBS-LRR Zhou et al., 2006
Pid-2 6 地谷 类受体激酶蛋白 Chen et al., 2006
Pid-3 6 地谷 NBS-LRR Shang et al., 2009
Pi-25 6 谷梅2号 NBS-LRR Chen et al., 2011
Pid3-A4 6 A4 (普通野生稻) NBS-LRR Lv et al., 2013
Pi50 6 Er-Ba-zhan (EBZ) NBS-LRR Zhu et al., 2012
Pigm 6 谷梅4号 NBS-LRR Deng et al., 2017
Pi-36 8 Q61 NBS-LRR Liu et al., 2007
Pi-5/Pi-3/Pii 9 Tetep NBS-LRR Lee et al., 2009
Pii 9 Hitomebore NBS-LRR Takagi et al., 2013
Pi56 9 三黄占2号 NBS-LRR Liu et al., 2013
Pikh/Pi-54 11 K3 NBS-LRR Sharma et al., 2005
Pik-m 11 Tsuyuake NBS-LRR Ashikawa et al., 2008
Pb1 11 Modan NBS-LRR Hayashi et al., 2010
Pik 11 Kusabue NBS-LRR Zhai et al., 2011
Pik-p 11 K60 NBS-LRR Yuan et al., 2011
Pia 11 Aichi Asahi NBS-LRR Hutin et al., 2016
Pi-1 11 LAC (根茎稻) NBS-LRR Hua et al., 2012
Pi54rh 11 nrcpb 002 NBS-LRR Das et al., 2012
Pi-CO39 11 CO39 (药用野生稻) NBS-LRR Chauhan et al., 2002
Pi54of 11 nrcpb004 NBS-LRR Devanna et al., 2014
PiK-h 11 K3 NBS-LRR Zhai et al., 2014
Pike 11 籼早143 NBS-LRR Chen et al., 2015
Piks 11 未知 NBS-LRR GenBank: AET36547.1
Pita 12 Yashiro-mochi NBS-LRR Bryan et al., 2000
Ptr 12 M2353 膜蛋白 Zhao et al., 2018

Table 3

Cloned avirulence genes of Magnaporthe oryzae"

无毒基因 供体菌株 对应R基因 功能 编码分
泌蛋白
参考文献
PWL1 WGG-FA40 未知 富含甘氨酸的带有信号肽的疏水蛋白 Kang et al., 1995
PWL2 Guy11 未知 富含甘氨酸的带有信号肽的疏水蛋白 Sweigard et al., 1995
PWL3 WGG-FA40 未知 富含甘氨酸的带有信号肽的疏水蛋白 Kang et al., 1995
PWL4 WGG-FA40 未知 富含甘氨酸的带有信号肽的疏水蛋白 Kang et al., 1995
Avr-CO39 K76-79 C039 功能未知, 仅在宿主细胞质中转录 Farman and Leong, 1998
Farman et al., 2002
Avr-Pita O-137 Pi-ta 含金属蛋白酶结构域, 作用于宿主细胞质 Orbach et al., 2000
ACE1 Guy11 Pi-33 编码一个非核糖体多聚乙酰合酶, 该酶参与代谢的产物能够被Pi-33识别并激活免疫反应 未知 Fudal et al., 2005
Avr-Pia Ina168 Pia 功能未知, 作用于宿主细胞质 Yoshida et al., 2009
Avr-Pii Ina168 Pii 功能未知, 作用于宿主细胞质 Yasuda et al., 2006
Avr-Pik/km/kp Ina168 Pik/km/kp 功能未知, 作用于宿主细胞质 Yoshida et al., 2009
Avr-Piz-t 81278ZB15 Piz-t 功能未知蛋白, 对基础抗性具有抑制作用 Li et al., 2009
Avr-Pi9 R01-1 Pi9 在水稻受到侵染时, 被转运到宿主细胞, 并且在侵染初期高表达 Wu et al., 2015
Avr-Pib CHL42 Pib 编码75个残基蛋白, 包括信号肽 Zhang et al., 2015b
Avr-Pita1 O-137 Pita1 产生16个功能蛋白 Takahashi et al., 2010a
AVR-Pi54 MG-79 Pi54 功能未知, 作用于宿主细胞质 Ray et al., 2016
BAS1, BAS2, BAS3, BAS4 O-137 未知 它们以不同的模式分泌到寄主细胞中, 但以相容方式互作 Mosquera et al., 2009
[1] 柏斌, 吴俊, 周波, 邓启云 ( 2012). 稻瘟病抗性分子育种研究综述. 杂交水稻 27, 5-9.
[2] 邓其明, 周鹏, 林琳, 王世全, 李双成, 李平 ( 2009). 水稻稻瘟病抗性基因研究进展及其在育种上的应用. 安徽农业科学 37, 1489-1492, 1508.
[3] 何秀英, 廖耀平, 陈钊明, 程永盛, 陈粤汉 ( 2011). 水稻稻瘟病抗病育种研究进展与展望. 广东农业科学 38, 30-33.
[4] 胡朝芹, 刘剑宇, 王韵茜, 杨睿, 汪秉琨, 何月秋, 曾千春, 罗琼 ( 2017). 粳稻子预44抗LP11稻瘟病菌基因Pizy6(t)的定位. 植物学报 52, 61-69.
[5] 柳武革, 王丰, 刘振荣, 朱小源, 李金华, 黄慧君, 廖亦龙, 朱满山, 付崇允, 陈建伟 ( 2012). 利用分子标记技术聚合Pi-1Pi-2基因改良三系不育系荣丰A的稻瘟病抗性. 分子植物育种 10, 575-582.
[6] 倪大虎, 易成新, 李莉, 汪秀峰, 张毅, 赵开军, 王春连, 章琦, 王文相, 杨剑波 ( 2008). 分子标记辅助培育水稻抗白叶枯病和稻瘟病三基因聚合系. 作物学报 34, 100-105.
[7] 文绍山, 高必军 ( 2012). 利用分子标记辅助选择将抗稻瘟病基因Pi-9(t)渗入水稻恢复系泸恢17. 分子植物育种 10, 42-47.
[8] 杨勤忠, 林菲, 冯淑杰, 王玲, 潘庆华 ( 2009). 水稻稻瘟病抗性基因的分子定位及克隆研究进展. 中国农业科学 42, 1601-1615.
[9] 易怒安, 李魏, 戴良英 ( 2015). 水稻抗稻瘟病基因的克隆及其分子育种研究进展. 分子植物育种 13, 1653-1659.
[10] 张佩胜, 赵春德, 余宁, 张迎信, 刘群恩 ( 2014). 稻瘟病抗性基因的克隆及应用研究进展. 中国稻米 20(5), 1-7.
doi: 10.3969/j.issn.1006-8082.2014.05.001
[11] 张晓慧, 冯晓敏, 林少扬 ( 2017). 水稻主栽品种空育131抗稻瘟病位点的扫描及其基因组重构建. 植物学报 52, 30-42.
[12] Roychowdhury M, 贾育林 , Cartwright RD ( 2013). 水稻抗稻瘟病基因的结构、功能和共同进化. 作物学报 38, 381-393.
[13] Ashikawa I, Hayashi N, Yamane H, Kanamori H, Wu JZ, Matsumoto T, Ono K, Yano M ( 2008). Two adjacent nucleotide-binding site-leucine-rich repeat class genes are required to confer Pikm -specific rice blast resistance. Genetics 180, 2267-2276.
[14] Brown JKM ( 2003). A cost of disease resistance: paradigm or peculiarity? Trends Genet 19, 667-671.
doi: 10.1016/j.tig.2003.10.008
[15] Bryan GT, Wu KS, Farrall L, Jia Y, Hershey HP, McAdams SA, Faulk KN, Donaldson GK, Tarchini R, 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.
[16] Cesari S ( 2018). Multiple strategies for pathogen perception by plant immune receptors. New Phytol 219, 17-24.
doi: 10.1111/nph.2018.219.issue-1
[17] Césari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V, Kawano Y, Shimamoto K, Dodds P, Terauchi R, Kroj T ( 2014). The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J 33, 1941-1959.
doi: 10.15252/embj.201487923
[18] Césari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y, Morel JB, Fournier E, Tharreau D, Terauchi R, Kroj T ( 2013). The rice resistance protein pair RGA4/RGA5 re- cognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25, 1643-1681.
[19] Chauhan RS, Farman ML, Zhang HB, Leong SA ( 2002). Genetic and physical mapping of a rice blast resistance locus, Pi-CO39(t), that corresponds to the avirulence gene AVR1-CO39 of Magnaporthe grisea. Mol Genet Genomics 267, 603-612.
[20] Chen J, Peng P, Tian JS, He YG, Zhang LP, Liu ZX, Yin DD, Zhang ZH ( 2015). Pike, a rice blast resistance allele consisting of two adjacent NBS-LRR genes, was identified as a novel allele at the Pik locus. Mol Breed 35, 117.
[21] Chen J, Shi YF, Liu WZ, Chai RY, Fu YP, Zhuang JY, Wu JL ( 2011). A Pid3 allele from rice cultivar Gumei2 confers resistance to Magnaporthe oryzae. J Genet Genomics 38, 209-216.
[22] Chen XW, Shang JJ, Chen DX, Lei CL, Zou Y, Zhai WX, Liu GZ, Xu JC, Ling ZZ, Cao G, Ma BT, Wang YP, Zhao XF, Li SG, Zhu LH ( 2006). A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46, 794-804.
doi: 10.1111/tpj.2006.46.issue-5
[23] Collier SM, Moffett P ( 2009). NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14, 521-529.
doi: 10.1016/j.tplants.2009.08.001
[24] Das A, Soubam D, Singh PK, Thakur S, Singh NK, Sharma TR ( 2012). A novel blast resistance gene, Pi54rh cloned from wild species of rice, Oryza rhizomatis confers broad spectrum resistance to Magnaporthe oryzae. Funct Integr Genomics 12, 215-228.
[25] Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW ( 2005). The genome sequence of the rice blast fungus Magnaporthe grisea . Nature 434, 980-986.
[26] Deng YW, Zhai KR, Xie Z, Yang DY, Zhu XD, Liu JZ, Wang X, Qin P, Yang YZ, Zhang GM, Li Q, Zhang JF, Wu SQ, Milazzo J, Mao BZ, Wang ET, Xie HA, Tharreau D, He ZH ( 2017). Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355, 962-965.
doi: 10.1126/science.aai8898
[27] Devanna NB, Vijayan J, Sharma TR ( 2014). The blast resistance gene Pi54of cloned from Oryza officinalis interacts with Avr-Pi54 through its novel non-LRR domains. PLoS One 9, e104840.
[28] Dodds PN, Rathjen JP ( 2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11, 539-548.
[29] Ebbole DJ ( 2007). Magnaporthe as a model for understanding host-pathogen interactions. Annu Rev Phytopathol 45, 437-456.
[30] Ezuka A ( 1972). Field resistance of rice varieties to blast disease. Rev Plant Prot Res 5, 1-21.
[31] Farman ML, Eto Y, Nakao T, Tosa Y, Nakayashiki H, Mayama S, Leong SA ( 2002). Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Mol Plant Microbe Interact 15, 6-16.
[32] Farman ML, Leong SA ( 1998). Chromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: discrepancy between the physical and genetic maps. Gene- tics 150, 1049-1058.
[33] Fudal I, Böhnert HU, Tharreau D, Lebrun MH ( 2005). Transposition of MINE, a composite retrotransposon, in the avirulence gene ACE1 of the rice blast fungus Magnaporthe grisea. Fungal Genet Biol 42, 761-772.
[34] Fujii K, Hayano-Saito Y, Saito K, Sugiura N, Hayashi N, Tsuji T, Izawa T, Iwasaki M ( 2000). Identification of a RFLP marker tightly linked to the panicle blast resistance gene, Pb1 , in rice. Breed Sci 50, 183-188.
[35] 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.
doi: 10.1126/science.1175550
[36] Fukuoka S, Yamamoto SI, 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.
[37] Hayashi K, Yoshida H, Ashikawa I ( 2006). Development of PCR-based allele-specific and InDel marker sets for nine rice blast resistance genes. Theor Appl Genet 113, 251-260.
doi: 10.1007/s00122-006-0290-6
[38] 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 th- rough local genome duplication. Plant J 64, 498-510.
[39] Hua LX, Wu JZ, Chen CX, Wu WH, He XY, Lin F, Wang L, Ashikawa I, Matsumoto T, Wang L, Pan QH ( 2012). The isolation of Pi1, an allele at the Pik locus which confers broad spectrum resistance to rice blast. Theor Appl Genet 125, 1047-1055.
[40] Hutin M, Césari S, Chalvon V, Michel C, Tran TT, Boch J, Koebnik R, Szurek B, Kroj T ( 2016). Ectopic activation of the rice NLR heteropair RGA4/RGA5 confers resistance to bacterial blight and bacterial leaf streak diseases. Plant J 88, 43-55.
doi: 10.1111/tpj.13231
[41] Jia YL, McAdams SA, Bryan GT, Hershey HP, Valent B ( 2000). Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19, 4004-4014.
doi: 10.1093/emboj/19.15.4004
[42] Jiang HC, Feng YT, Bao L, Li X, Gao GJ, Zhang QL, Xiao JH, Xu CG, He YQ ( 2012a). Improving blast resistance of Jin 23B and its hybrid rice by marker-assisted gene pyramiding. Mol Breed 30, 1679-1688.
doi: 10.1007/s11032-012-9751-6
[43] Jiang N, Li ZQ, Wu J, Wang Y, Wu LQ, Wang SH, Wang D, Wen T, Liang Y, Sun PY, Liu JL, Dai LY, Wang ZL, Wang C, Luo MZ, Liu XL, Wang GL ( 2012b). Molecular mapping of the Pi2/9 allelic gene Pi2-2 conferring broad- spectrum resistance to Magnaporthe oryzae in the rice cultivar Jefferson. Rice 5, 29.
[44] Jones JDG, Dangl JL ( 2006). The plant immune system. Nature 444, 323-329.
doi: 10.1038/nature05286
[45] Kang S, Sweigard JA, Valent B ( 1995). The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 8, 939-948.
[46] Keen NT ( 1990). Gene-for-gene complentarity in plant- pathogen interaction. Annu Rev Genet 24, 447-463.
doi: 10.1146/annurev.ge.24.120190.002311
[47] Khan M, Subramaniam R, Desveaux D ( 2016). Of guards, decoys, baits and traps: pathogen perception in plants by type III effector sensors. Curr Opin Microbiol 29, 49-55.
doi: 10.1016/j.mib.2015.10.006
[48] Khush GS ( 2005). What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol 59, 1-6.
doi: 10.1007/s11103-005-2159-5
[49] Kiyosawa S ( 1989). Breakdown of blast resistance in rice in relation to general strategies of resistance gene deployment to prolong effectiveness of disease resistance in plants. In: Leonard KJ, Fry WE, eds. Plant Disease Epidemiology. New York: McGraw-Hill. pp. 251-283.
[50] Lee SK, Song MY, Seo YS, Kim HK, Ko S, Cao PJ, Suh JP, Yi G, Roh JH, Lee S, An G, Hahn TR, Wang GL, Ronald P, Jeon JS ( 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.
[51] Li JB, Li D, Sun YD, Xu MH ( 2012). Rice blast resistance gene Pi1 identified by MRG4766 marker in 173 Yunnan rice landraces. Rice Genom Genet 3, 13-18.
[52] Li JB, Sun YD, Liu H, Wang YY, Jia YL, Xu MH ( 2015). Natural variation of rice blast resistance gene Pi-d2 . Genet Mol Res 14, 1235-1249.
[53] Li W, Wang BH, Wu J, Lu GD, Hu YJ, Zhang X, Zhang ZG, Zhao Q, Feng Q, Zhang HY, Wang ZY, Wang GL, Han B, Wang ZH, Zhou B ( 2009). The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant Microbe Interact 22, 411-420.
[54] Li WT, Zhu ZW, Chern M, Yin JJ, Yang C, Ran L, Cheng MP, He M, Wang K, Wang J, Zhou XG, Zhu XB, Chen ZX, Wang JC, Zhao W, Ma BT, Qin P, Chen WL, Wang YP, Liu JL, Wang WM, Wu XJ, Li P, Wang JR, Zhu LH, Li SG, Chen XW ( 2017). A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170, 114-126.
doi: 10.1016/j.cell.2017.06.008
[55] Lin F, Chen S, Que ZQ, Wang L, Liu XQ, Pan QH ( 2007). The blast resistance gene Pi37 encodes a Nucleotide Binding Site-Leucine-Rich repeat protein and is a member of a resistance gene cluster on rice chromosome 1. Genetics 177, 1871-1880.
[56] Liu XQ, Lin F, Wang L, Pan Q ( 2007). The in Silico map- based cloning of Pi36, a rice Coiled-Coil-Nucleotide- Binding Site-Leucine-Rich Repeat gene that confers race-specific resistance to the blast fungus. Genetics 176, 2541-2549.
[57] Liu Y, Liu B, Zhu XY, Yang JY, Bordeos A, Wang GL, Leach JE, Leung H ( 2013). Fine-mapping and molecular marker development for Pi56(t), a NBS-LRR gene conferring broad-spectrum resistance to Magnaporthe oryzae in rice. Theor Appl Genet 126, 985-998.
[58] Liu YL, Schiff M, Serino G, Deng XW, Dinesh-Kumar SP ( 2002). Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to Tobacco mosaic virus. Plant Cell 14, 1483-1496.
[59] Lv QM, Xu X, Shang JJ, Jiang GH, Pang ZQ, Zhou ZZ, Wang J, Liu Y, Li T, Li XB, Xu JC, Cheng ZK, Zhao XF, Li SG, Zhu LH ( 2013). Functional analysis of Pid3-A4, an ortholog of rice blast resistance gene Pid3 revealed by allele mining in common wild rice. Phytopathology 103, 594-599.
[60] Ma J, Lei CL, Xu XT, Hao K, Wang JL, Cheng ZJ, Ma XD, Ma J, Zhou KN, Zhang X, Guo XP, Wu FQ, Lin QB, Wang CM, Zhai HQ, Wang HY, Wan JM ( 2015). Pi64, encoding a novel CC-NBS-LRR protein, confers resistance to leaf and neck blast in rice. Mol Plant Microbe Interact 28, 558-568.
[61] Mosquera G, Giraldo MC, Hyun Khang C, Coughlan S, Valent B ( 2009). Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as Biotrophy-Associated secreted proteins in rice blast disease. Plant Cell 21, 1273-1290.
[62] Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT, Pevzner SJ, Donovan SE, Ghamsari L, Santhanam B, Romero V, Poulin MM, Gebreab F, Gutierrez BJ, Tam S, Monachello D, Boxem M, Harbort CJ, McDonald N, Gai LT, Chen HM, He YJ, European Union Effectoromics Consortium, Vandenhaute J, Roth FP, Hill DE, Ecker R, Vidal M, Beynon J, Braun P, Dangl JL ( 2011). Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596-601.
doi: 10.1126/science.1203659
[63] Nelson R, Wiesner-Hanks T, Wisser R, Balint-Kurti P ( 2018). Navigating complexity to breed disease-resistant crops. Nat Rev Genet 19, 21-33.
[64] Nguyen TTT, Koizumi S, La TN, Zenbayashi KS, Ashizawa T, Yasuda N, Imazaki I, Miyasaka A ( 2006). Pi35(t), a new gene conferring partial resistance to leaf blast in the rice cultivar Hokkai 188. Theor Appl Genet 113, 697-704.
[65] Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B ( 2000). A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta . Plant Cell 12, 2019-2032.
[66] Ortiz D, de Guillen K, Cesari S, Chalvon V, Gracy J, Padilla A, Kroj T ( 2017). Recognition of the Magnaporthe oryzae effector AVR-Pia by the decoy domain of the rice NLR immune receptor RGA5. Plant Cell 29, 156-168.
[67] Qu SH, Liu GF, Zhou B, Bellizzi M, Zeng LR, Dai LY, Han B, Wang GL ( 2006). The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics 172, 1901-1914.
[68] Ray S, Singh PK, Gupta DK, Mahato AK, Sarkar C, Rathour R, Singh NK, Sharma TR ( 2016). Analysis of Magnaporthe oryzae genome reveals a fungal effector, which is able to induce resistance response in transgenic rice line containing resistance gene, Pi54. Front Plant Sci 7, 1140.
[69] Shang JJ, Tao Y, Chen XW, Zou Y, Lei CL, Wang J, Li XB, Zhao XF, Zhang MJ, Lu ZK, Xu JC, Cheng ZK, Wan JM, Zhu LH ( 2009). Identification of a new rice blast resistance gene, Pid3 , by genomewide comparison of paired nucleotide-binding site-leucine-rich repeat genes and their pseu- dogene alleles between the two sequenced rice genomes. Genetics 182, 1303-1311.
[70] Sharma TR, Madhav MS, Singh BK, Shanker P, Jana TK, Dalal V, Pandit A, Singh A, Gaikwad K, Upreti HC, Singh NK ( 2005). High-resolution mapping, cloning and molecular characterization of the Pi-k h gene of rice, which confers resistance to Magnaporthe grisea. Mol Genet Geno- mics 274, 569-578.
[71] Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, Valent B ( 1995). Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7, 1221-1233.
[72] Takagi H, Uemura A, Yaegashi H, Tamiru M, Abe A, Mit- suoka C, Utsushi H, Natsume S, Kanzaki H, Matsumura H, Saitoh H, Yoshida K, Cano LM, Kamoun S, Terauchi R ( 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.
[73] Takahashi M, Ashizawa T, Hirayae K, Moriwaki J, Sone T, Sonoda R, Noguchi MT, Nagashima S, Ishikawa K, Arai M ( 2010a). One of two major paralogs of AVR-Pita1 is functional in Japanese rice blast isolates. Phytopathology 100, 612-618.
[74] Takahashi A, Hayashi N, Miyao A, Hirochika H ( 2010b). Unique features of the rice blast resistance Pish locus revealed by large scale retrotransposon-tagging. BMC Plant Biol 10, 175.
[75] Takahashi JS, Pinto LH, Vitaterna MH ( 1994). Forward and reverse genetic approaches to behavior in the mouse. Science 264, 1724-1733.
doi: 10.1126/science.8209253
[76] Van der Hoorn RA, Kamoun S ( 2008). From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009-2017.
doi: 10.1105/tpc.108.060194
[77] Wang BH, Ebbole DJ, Wang ZH ( 2017). The arms race between Magnaporthe oryzae and rice: diversity and interaction of Avr and R genes. J Integr Agric 16, 2746-2760.
[78] 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.
[79] Wang J, Zhou LA, Shi H, Chern M, Yu H, Yi H, He M, Yin JJ, Zhu XB, Li Y, Li WT, Liu JL, Wang JC, Chen XQ, Qing H, Wang YP, Liu GF, Wang WM, Li P, Wu XJ, Zhu LH, Zhou JM, Ronald PC, Li SG, Li JY, Chen XW ( 2018). A single transcription factor promotes both yield and immunity in rice. Science 361, 1026-1028.
doi: 10.1126/science.aat7675
[80] Wang RY, Ning YS, Shi XT, He F, Zhang CY, Fan JB, Jiang N, Zhang Y, Zhang T, Hu YJ, Bellizzi M, Wang GL ( 2016). Immunity to rice blast disease by suppression of effector-triggered necrosis. Curr Biol 26, 2399-2411.
doi: 10.1016/j.cub.2016.06.072
[81] Wang X, Richards J, Gross T, Druka A, Kleinhofs A, Steffenson B, Acevedo M, Brueggeman R ( 2013). The rpg4-mediated resistance to wheat stem rust( Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor. Mol Plant Microbe Interact 26, 407-418.
[82] Wang ZX, Yano M, Yamanouchi U, Iwamoto M, Monna L, Hayasaka H, Katayose Y, Sasaki T ( 1999). The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J 19, 55-64.
[83] Wu J, Kou YJ, Bao JD, Li Y, Tang MZ, Zhu XL, Ponaya A, Xiao G, Li JB, Li CY, Song MY, Cumagun CJR, Deng QY, Lu GD, Jeon JS, Naqvi NI, Zhou B ( 2015). Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytol 206, 1463-1475.
[84] Xu X, Hayashi N, Wang CT, Fukuoka S, Kawasaki S, Takatsuji H, Jiang CJ ( 2014). Rice blast resistance gene Pikahei-1( t), a member of a resistance gene cluster on chromosome 4, encodes a nucleotide-binding site and leucine-rich repeat protein. Mol Breed 34, 691-700.
[85] Xu YB, McCouch SR, Zhang QF ( 2005). How can we use genomics to improve cereals with rice as a reference genome? Plant Mol Biol 59, 7-26.
doi: 10.1007/s11103-004-4681-2
[86] Yasuda N, Mitsunaga T, Hayashi K, Koizumi S, Fujita Y ( 2015). Effects of pyramiding quantitative resistance genes pi21, Pi34, and Pi35 on rice leaf blast disease. Plant Dis 99, 904-909.
[87] Yasuda N, Noguchi MT, Fujita Y ( 2006). Partial mapping of avirulence genes AVR-Pii and AVR-Pia in the rice blast fun- gus Magnaporthe oryzae. Can J Plant Pathol 28, 494-498.
[88] Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Yoshida K, Tosa Y, Chuma I, Takano Y, Win J, Kamoun S, Terauchi R ( 2009). Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae . Plant Cell 21, 1573-1591.
[89] Yu ZH, Mackill DJ, Bonman JM, McCouch SR, Guiderdoni E, Notteghem JL, Tanksley SD ( 1996). Molecular mapping of genes for resistance to rice blast ( Pyricularia grisea Sacc.). Theor Appl Genet 93, 859-863.
[90] Yuan B, Zhai C, Wang WJ, Zeng XS, Xu XK, Hu HQ, Lin F, Wang L, Pan QH ( 2011). The Pik-p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes. Theor Appl Genet 122, 1017-1028.
[91] Zenbayashi-Sawata K, Fukuoka S, Katagiri S, Fujisawa M, Matsumoto T, Ashizawa T, Koizumi S ( 2007). Genetic and physical mapping of the partial resistance gene, Pi34 , to blast in rice. Phytopathology 97, 598-602.
[92] Zhai C, Lin F, Dong ZQ, He XY, Yuan B, Zeng XS, Wang L, Pan QH ( 2011). The isolation and characterization of Pik , a rice blast resistance gene which emerged after rice domestication. New Phytol 189, 321-334.
[93] Zhai C, Zhang Y, Yao N, Lin F, Liu Z, Dong ZQ, Wang L, Pan QH ( 2014). Function and interaction of the coupled genes responsible for Pik-h encoded rice blast resistance. PLoS One 9, e98067.
[94] Zhang N, Luo J, Rossman AY, Aoki T, Chuma I, Crous PW, Dean R, de Vries RP, Donofrio N, Hyde KD, Lebrun MH, Talbot NJ, Tharreau D, Tosa Y, Valent B, Wang ZH, Xu JR ( 2016). Generic names in Magnaporthales . IMA Fungus 7, 155-159.
[95] Zhang XH, Yang SH, Wang J, Jia YX, Huang J, Tan SJ, Zhong Y, Wang L, Gu LJ, Chen JQ, Pan QH, Bergelson J, Tian DC ( 2015a). A genome-wide survey reveals abundant rice blast R genes in resistant cultivars. Plant J 84, 20-28.
[96] Zhang SL, Wang L, Wu WH, He LY, Yang XF, Pan QH ( 2015b). Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib. Sci Rep 5, 11642.
[97] Zhao HJ, Wang XY, Jia YL, Minkenberg B, Wheatley M, Fan JB, Jia MH, Famoso A, Edwards JD, Wamishe Y, Valent B, Wang GL, Yang YN ( 2018). The rice blast resistance gene Ptr encodes an atypical protein required for broad-spectrum disease resistance. Nat Commun 9, 2039.
[98] Zhou B, Qu SH, Liu GF, Dolan M, Sakai H, Lu GD, Bellizzi M, Wang GL ( 2006). The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea . Mol Plant Microbe Interact 19, 1216-1228.
[99] Zhou JM, Chai JJ ( 2008). Plant pathogenic bacterial type III effectors subdue host responses. Curr Opin Microbiol 11, 179-185.
doi: 10.1016/j.mib.2008.02.004
[100] Zhu XY, Chen S, Yang JY, Zhou SC, Zeng LX, Han JL, Su J, Wang L, Pan QH ( 2012). The identification of Pi50(t), a new member of the rice blast resistance Pi2/Pi9 multigene family. Theor Appl Genet 124, 1295-1304.
[1] yuchun Rao. Research Progress on Rice Root Genetics and Breeding [J]. Chin Bull Bot, 2020, 55(3): 0-0.
[2] Chen Xifeng,Liu Yaping,Ma Bojun. Design and Practice of a New Teaching Project of the Map-based Cloning Experiment in Genetics [J]. Chin Bull Bot, 2019, 54(6): 797-803.
[3] Zhou Chun, Jiao Ran, Hu Ping, Lin Han, Hu Juan, Xu Na, Wu Xianmei, Rao Yuchun, Wang Yuexing. Gene Mapping and Candidate Gene Analysis of Rice Early Senescence Mutant LS-es1 [J]. Chin Bull Bot, 2019, 54(5): 606-619.
[4] Wang Yunqian, Su Yanhong, Yang Rui, Li Xin, Li Jing, Zeng Qianchun, Luo Qiong. Rice Blast Resistance of Wild Rice in Yunnan [J]. Chin Bull Bot, 2018, 53(4): 477-486.
[5] Yuan Cao, Yun Yang, Huaquan Xu, Yang Liu, Danyang Wan. PCR Used to Find Plasmid Backbone Fragments in the Products of hiTAIL-PCR [J]. Chin Bull Bot, 2018, 53(1): 104-109.
[6] Li Ma, Wancang Sun, Jinhai Yuan, Zigang Liu, Junyan Wu, Yan Fang, Yaozhao Xu, Yuanyuan Pu, Jing Bai, Xiaoyun Dong, Huili He. Expression Analysis of β-1,3-Glucanase Gene from Winter Brassica rapa Under Low Temperature Stress [J]. Chin Bull Bot, 2017, 52(5): 568-578.
[7] Zhengjun Xia. Research Progress in Whole-genome Analysis and Cloning of Genes Underlying Important Agronomic Traits in Soybean [J]. Chin Bull Bot, 2017, 52(2): 148-158.
[8] Hu Chaoqin, , Liu Jianyu, , Wang Yunqian, Yang Rui, Wang Bingkun, He Yueqiu, Zeng Qianchun, Luo Qiong. Mapping of Pizy6(t), a Gene Conferring Resistance to the Rice Blast Strain LP11, in Oryza sativa subsp. japonica Cultivar Ziyu44 [J]. Chin Bull Bot, 2017, 52(1): 61-69.
[9] Wang Wenle, Feng Dan, Wu Jinxia, Zhang Zhiguo, Lu Tiegang. Gene Mapping of a Dwarf Gene WLD1 in Rice [J]. Chin Bull Bot, 2017, 52(1): 54-60.
[10] Xiaohui Zhang, Xiaomin Feng, Shaoyang Lin. Scanning for Pi Loci and Rebuilding an Improved Genome of Elite Rice Variety Kongyu 131 [J]. Chin Bull Bot, 2017, 52(1): 30-42.
[11] Juqing Kang, Tianshu Sun, Huiting Zhang, Yihao Shi. Quantitative Trait Loci Mapping Platform of Natural Populations of Arabidopsis thaliana along the Yangtze River in China [J]. Chin Bull Bot, 2016, 51(5): 659-666.
[12] Wei Wang, Jiayu Wang, Shenglong Yang, Jin Liu, Xiaoyan Dong, Guojiao Wang, Wenfu Chen. Identification and Gene Mapping of the nrl7 Mutant in Rice [J]. Chin Bull Bot, 2016, 51(3): 290-295.
[13] Danlong Jing, Yan Xia, Shougong Zhang, Junhui Wang. Expression Analysis of B-class MADS-box Genes from Catalpa speciosa [J]. Chin Bull Bot, 2016, 51(2): 210-217.
[14] Qinghua Guo, Jin Liu, Yumei Li, Qiuping Zhai, Yongcai Wang, Fangfang Wu, Tianyu Hu, Huawei Wan, Huiming Liu, Wenming Shen. A near-surface remote sensing platform for biodiversity monitoring: perspectives and prospects [J]. Biodiv Sci, 2016, 24(11): 1249-1266.
[15] Yongshu Liang, Junjie Zhou, Wenbin Nan, Dongdong Duan, Hanma Zhang. Progress in Rice Root System Research [J]. Chin Bull Bot, 2016, 51(1): 98-106.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] LIU Jun;ZHAO Lan-Yong;FENG Zhen;ZHANG Mei-Rong;WU Yin-Feng. Optimization Selection of Genetic Transformation Regeneration System from Leaves of Dendranthema morifolium[J]. Chin Bull Bot, 2004, 21(05): 556 -558 .
[2] Luo Jian-ping and Ja Jing-fen. Structure and Function of Plant Oligosaceaharins[J]. Chin Bull Bot, 1996, 13(04): 28 -33 .
[3] YANG Qi-He SONG Song-Quan YE Wan-HuiYIN Shou-HuaT. Mechanism of Seed Photosensitivity and FactorsInfluencing Seed Photosensitivity[J]. Chin Bull Bot, 2003, 20(02): 238 -247 .
[4] CUI Yue-Hua;WANG Mao and SUN Ke-Lian. Morphological Study of Gutta-containing Cells in Eucommia ulmoides Oliv.[J]. Chin Bull Bot, 1999, 16(04): 439 -443 .
[5] CHEN Shao-Liang LI Jin-Ke BI Wang-Fu WANG Sha-Sheng. Genotypic Variation in Accumulation of Salt Ions, Betaine and Sugars in Poplar Under Conditions of Salt Stress[J]. Chin Bull Bot, 2001, 18(05): 587 -596 .
[6] . Advances in Research into Low-Phytic-Acid Mutants in Crops[J]. Chin Bull Bot, 2005, 22(04): 463 -470 .
[7] Cong Ma, Weiwen Kong. Research Progress in Plant Metacaspase[J]. Chin Bull Bot, 2012, 47(5): 543 -549 .
[8] Chang’en Tian, Yuping Zhou. Research Progress in Plant IQ Motif-containing Calmodulin-binding Proteins[J]. Chin Bull Bot, 2013, 48(4): 447 -460 .
[9] Huawei Xu, Dianyun Hou. Research Advances in Protein Transport into Chloroplasts in Plant Cell#br#[J]. Chin Bull Bot, 2018, 53(2): 264 -275 .
[10] Li Jiandong, Zheng Huiying. ?ber die Anwendung der Braun-Blanquet's Methode in der Steppen-Untersuchung[J]. Chin J Plan Ecolo, 1983, 7(3): 186 -203 .