The arms race between Magnaporthe oryzae and rice: Diversity and interaction of Avr and R genes

doi:10.1016/S2095-3119(17)61746-5

摘要/Abstract

Abstract: Rice blast disease, caused by Magnaporthe oryzae, threatens global food security. The rice blast pathosystem is a longstanding model system for understanding plant-microbe interactions. In order to elucidate the coevolution of the host and pathogen, and provide the appropriate methods for preventing or controlling rice blast disease, researchers have focused on the evolution of virulence factors and resistance genes. Thus far, more than 30 rice blast resistance (R) genes and 12 avirulence (Avr) genes have been cloned. This review summarizes the cloned rice blast R genes, cloned Avr genes of M. oryzae and the interaction between them. This discussion also considers some of the major unanswered questions concerning this pathosystem and the opportunities for future investigations.

Key words: rice , Maganporthe oryzae , resistance gene , avirulence gene , co-evolution , genetic diversity

. [J]. Journal of Integrative Agriculture, 2017, 16(12): 2746-2760.

WANG Bao-hua, Daniel J. Ebbole, WANG Zong-hua. The arms race between Magnaporthe oryzae and rice: Diversity and interaction of Avr and R genes[J]. Journal of Integrative Agriculture, 2017, 16(12): 2746-2760.

参考文献

Ahn S N, Kim Y K, Hong H C, Han S, Kwon S J, Choi H C, Moon H P, McCouch S R. 2000. Molecular mapping of a new gene for resistance to rice blast (Pyricularia grisea Sacc.). Euphytica, 116, 17–22.

Ashikawa I, Hayashi N, Yamane H, Kanamori H, Wu J, 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.

Van der Biezen E A, Jones J D G. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends in Plant Science, 23, 454–456.

Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L, Narusaka Y, Reymond M, Parker J E, O’Connell R. 2009. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. The Plant Journal, 60, 602–613.

Böhnert H U, Fudal I, Dioh W, Tharreau D, Notteghem J L, Lebrun M H. 2004. A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. The Plant Cell, 16, 2499–2513.

Bryan G T, Wu K S, Farrall L, Jia Y, Hershey H P, McAdams S A, Faulk K N, Donaldson G K, Tarchini R, Valent B. 2000. A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. The Plant Cell, 12, 2033–2046.

Callaway E. 2016. Devastating wheat fungus appears in Asia for the first time. Nature, 543, 421–422.

Cesari 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. The EMBO Journal, 33, 1941–59.

Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y, Jean-Benoit-Morel Fournier E, Tharreau D, Terauchi R, Kroja T. 2013. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. The Plant Cell, 25, 1463–1481.

Chen J, Peng P, Tian J, He Y, Zhang L, Liu Z, Yin D, Zhang Z. 2015. Pike, a rice blast resistance allele consisting of two adjacent NBS-LRR genes, was identified as a novel allele at the Pik locus. Molecular Breeding, 35, 117.

Chen J, Shi Y F, Liu W, Chai R, Fu Y, Zhuang J, Wu J. 2011. A Pid3 allele from rice cultivar Gumei2 confers resistance to Magnaporthe oryzae. Journal of Genetics and Genomics, 38, 209–216.

Chen Q, Wang Y, Li A, Zhang Z, Zheng X. 2007. Molecular mapping of two cultivar-specific avirulence genes in the rice blast fungus Magnaporthe grisea. Molecular Genetics and Genomics, 277, 139–148.

Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L. 2006. A B-lectin receptor kinase gene conferring rice blast resistance. The Plant Journal, 46, 794–804.

Chisholm S T, Coaker G, Day B, Staskawicz B J. 2006. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell, 124, 803–814.

Dangl J L, Jones J D. 2001. Plant pathogens and integrated defence responses to infection. Nature, 411, 826–833.

Das A, Soubam D, Singh P K, Thakur S, Singh N K, Sharma T R. 2012. A novel blast resistance gene, Pi54rh cloned from wild species of rice, Oryza rhizomatis confers broad spectrum resistance to Magnaporthe oryzae. Functional & Integrative Genomics, 12, 215–228.

Deng Y, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G, Li Q, Zhang J, Wu S, Milazzo J, Mao B, Wang E, Xie H, Tharreau D, He Z. 2017. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science, 355, 962–965.

Devanna N B, Vijayan J, Sharma T R. 2014. The blast resistance gene Pi54of cloned from Oryza officinalis interacts with Avr-Pi54 through its novel non-LRR domains. PLoS ONE, 9, e104840.

Ding X, Richter T, Chen M, Fujii H, Seo YS, Xie M, Zheng X, Kanrar S, Stevenson R A, Dardick C, Li Y, Jiang H, Zhang Y, Yu F, Bartley L E, Chern M, Bart R, Chen X, Zhu L, Farmerie W G, Gribskov M, et al. 2009. A rice kinase-protein interaction map. Plant Physiology, 149, 1478–1492.

Dodds P N, Rathjen J P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nature Review Genetics, 11, 539–548.

Du Y, Mpina M, Birch P, Bouwmeester K, Govers F. 2015. Phytophthora infestans RXLR effector AVR1 interacts with exocyst component sec5 to manipulate plant immunity. Plant Physiology, 169, 1975–1990.

Elert E. 2014. Outlook rice: A good grain. Nature, 514, S50–S51.

Farman M L, Eto Y, Nakao T, Tosa Y, Nakayashiki H, Mayama S, Leong S A. 2002. Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Molecular Plant-Microbe Interactions, 15, 6–16.

Farman M, Peterson G, Chen L, Starnes J, Valent B, Bachi P, Murdock L, Hershman D, Pedley K, Fernandes J M, Bavaresco J. 2017. The Lolium pathotype of Magnaporthe oryzae recovered from a single blasted wheat plant in the United States. Plant Disease, 101, 684–692.

Farman M L, Leong S A. 1998. Chromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: Discrepancy between the physical and genetic maps. Genetics, 150, 1049–1058.

Fjellstrom R, McClung A M, Shank A R. 2006. SSR markers closely linked to the Pi-z locus are useful for selection of blast resistance in a broad array of rice germplasm. Molecular Breeding, 17, 149–157.

Fujisaki K, Abe Y, Ito A, Saitoh H, Yoshida K, Kanzaki H, Kanzaki E, Utsushi H, Yamashita T, Kamoun S, Terauchi R. 2015. Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity. The Plant Journal, 83, 875–887.

Flor H H. 1971. Current status of the gene-for-gene concept. Annual Review of Phytopathology, 9, 275–296.

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 I, Mizobuchi R, Yamanouchi U, Ono K, Kitazawa N, Yasuda N, Fujita Y, Nguyen T T, 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. Scientific Reports, 4, 1–7.

González-Lamothe R, Tsitsigiannis D I, Ludwig A A, Panicot M, Shirasu K, Jones J D. 2006. The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. The Plant Cell, 18, 1067–1083.

de Guillen K, Ortiz-Vallejo D, Gracy J, Fournier E, Kroj T, Padilla A. 2015. Structure analysis uncovers a highly diverse but structurally conserved effector family in phytopathogenic fungi. PLoS Pathogens, 11, e1005228.

Hayashi K, Yoshida H. 2009. Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. The Plant Journal, 57, 413–425.

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 restsistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. The Plant Journal, 64, 498–510.

Hua L, Wu J, Chen C, Wu W, He X, Lin F, Wang L, Ashikawa I, Matsumoto T, Wang L, Pan Q. 2012. The isolation of Pi1, an allele at the Pik locus which confers broad spectrum resistance to rice blast. Theoretical and Applied Genetics, 125, 1047–1055.

Inoue Y, Vy T T P, Yoshida K, Asano H, Mitsuoka C, Asuke S, Anh V L, Cumagun C J R, Chuma I, Terauchi R, Kato K, Mitchell T, Valent B, Farman M, Tosa Y. 2017. Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science, 357, 80–83.

Inukai T, Nelson R J, Ziegler R S, Sarkarung S, Mackill D J, Bonman J M, Takamure I, Kinoshita T. 1994. Allelism of blast resistance genes in near-isogenic lines of rice. Phytopathology, 84, 1278–1283.

Ishikawa K, Yamaguchi K, Sakamoto K, Yoshimura S, Inoue K, Tsuge S, Kojima C, Kawasaki T. 2014. Bacterial effector modulation of host E3 ligase activity suppresses PAMP-triggered immunity in rice. Nature Communications, 5, 5430.

Islam M T, Croll D, Gladieux P, Soanes D M, Persoons A, Bhattacharjee P, Hossain M S, Gupta D R, Rahman M M, Mahboob M G, Cook N, Salam M U, Surovy M Z, Sancho V B, Maciel J L, NhaniJúnior A, Castroagudín V L, Reges J T, Ceresini P C, Ravel S, et al. 2016. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biology, 14, 84.

Jeung J, Kim B, Cho Y, Han S, Moon H, Lee Y, Jena K. 2007. A novel gene, Pi40(t), linked to the DNA markers derived from NBS-LRR motifs confers broad spectrum of blast resistance in rice. Theoretical and Applied Genetics, 115, 1163–1177.

Jia Y, McAdams S A, Bryan G T, Hershey H P, Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. The EMBO Journal, 19, 4004–4014.

Jiang N, Li Z, Wu J, Wang Y, Wu L, Wang S, Wang D, Wen T, Liang Y, Sun P, Liu J, Dai L, Wang Z, Wang C, Luo M, Liu X, Wang G. 2012. 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.

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

Kang S, Sweigard J A, Valent B. 1995. The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Molecular Plant-Microbe Interactions, 8, 939–948.

Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, Fournier E, Tharreau D, Terauchi R. 2012. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. The Plant Journal, 72, 894–907.

Khang C, Park S, Lee Y, Valent B, Kang S. 2008. Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Molecular Plant-Microbe Interactions, 21, 658–670.

Kim Y J, Lin N C, Martin G B. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell, 109, 589–598.

Kohli M, Mehta Y, Guzman E, Viedma L, Cubilla L. 2011. Pyricularia blast - A threat to wheat cultivation. Czech Journal of Genetics and Plant Breeding, 47, S130–S134.

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, An G, Hahn T R, Wang G L, Ronald P, Jeon J S. 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.

Li P, Dong B, Zhou H, Zhou B. 2012. Functional analysis of cysteine residues of the Magnaporthe oryzae avirulence protein AvrPiz-t. Acta Phytopathologica Sinica, 42, 474–479.

Li W, Wang B, Wu J, Lu G, Hu Y, Zhang X, Zhang Z, Zhao Q, Feng Q, Zhang H, Wang Z, Wang G, Han B, Wang Z, 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. Molecular Plant-Microbe Interactions, 22, 411–420.

Li W, Zhong S, Li G, Li Q, Mao B, Deng Y, Zhang H, Zeng L, Song F, He Z. 2011. Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence. Cell Research, 21, 835–848.

Lin F, Chen S, Que Z, Wang L, Liu X, Pan Q. 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.

Liu J, Li W, Ning Y, Shirsekar G, Cai Y, Wang X, Dai L, Wang Z, Liu W, Wang G. 2012. The U-Box E3 ligase SPL11/PUB13 is a convergence point of defense and flowering signaling in plants. Plant Physiology, 160, 28–37.

Liu J, Wang X, Mitchell T, Hu Y, Liu X, Dai L, Wang G. 2010. Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. Molecular Plant Pathology, 11, 419–427.

Liu X, 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.

Liu Y, Liu B, Zhu X, Yang J, Bordeos A, Wang G, Leach J E, 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. Theoretical and Applied Genetics, 126, 985–998.

Lü Q, Xu X, Shang J, Jiang G, Pang Z, Zhou Z, Wang J, Liu Y, Li T, Li X, Xu J, Cheng Z, Zhao X, Li S, Zhu L. 2013. Functional analysis of Pid3-A4, anortholog of rice blast resistance gene Pid3 revealed by allele mining in common wild rice. Phytopathology, 103, 594–599.

Ma J, Lei C, Xu X, Hao K, Wang J, Cheng Z, Ma X, Ma J, Zhou K, Zhang X, Guo X, Wu F, Lin Q, Wang C, Zhai H, Wang H, Wan J. 2015. Pi64, encoding a novel CC-NBS-LRR protein, confers resistance to leaf and neck blast in rice. Molecular Plant-Microbe Interactions, 28, 558–568.

Malaker P K, Barma N C D, Tiwari T P,Collis W J, Duveiller E, Singh P K, Joshi A K Singh R P, Braun H J, Peterson G L, Pedley K F, Farman M L, Valent B. 2016. First report of wheat blast caused by Magnaporthe oryzae pathotype triticum in Bangladesh. Plant Disease, 100, 2330.

Maqbool A, Saitoh H, Franceschetti M, Stevenson C E, Uemura A, Kanzaki H, Kamoun S, Terauchi R, Banfield M J. 2015. Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. eLife, 4, e08709.

Martin G B. Bogdanove A J. Sessa G. 2003. Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology, 54, 23–61.

Miki S, Matsui K, Kito H, Otsuka K, Ashizawa T, Yasuda N, Fukiya S, Sato J, Hirayae K, Fujita Y, Nakajima T, Tomita F, Sone T. 2009. Molecular cloning and characterization of the AVR-Pia locus from a Japanese field isolate of Magnaporthe oryzae. Molecular Plant Pathology, 10, 361–374.

Mucyn T, Clemente A, Andriotis V, Balmuth A, Oldroyd G, Staskawicz B, Rathjen J. 2006. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. The Plant Cell, 18, 2792–2806.

Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, Narusaka Y. 2009. RRS1 and RPS4 provide a dual resistance-gene system against fungal and bacterial pathogens. The Plant Journal, 60, 218–226.

Nyarko A, Singarapu K, Figueroa M, Manning V, Pandelova I, Wolpert T J, Ciuffetti L M, Barbar E. 2014. Solution NMR structures of Pyrenophora tritici-repentis ToxB and its inactive homolog reveal potential determinants of toxin activity. The Journal of Biological Chemistry, 289, 25946–25956.

Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M, Saitoh H, Fujibe T, Matsumura H, Shenton M, Galam D C, Undan J, Ito A, Sone T, Terauchi R. 2011. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. The Plant Journal, 66, 467–479.

Orbach M J, Farrall L, Sweigard J A, Chumley F G, Valent B. 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. The Plant Cell, 12, 2019–2032.

Ose T, Oikawa A, Nakamura Y, Maenaka K, Higuchi Y, Satoh Y, Fujiwara S, Demura M, Sone T, Kamiya M. 2015. Solution structure of an avirulence protein, AVR-Pia, from Magnaporthe oryzae. Journal of Biomolecular NMR, 63, 229–235.

Pan H Q, Tanisaka T, Ikehashi H. 1996. Studies on the genetics and breeding of blast resistance in rice VI. Gene analysis of the blast resistance of two Yunnan native cultivars GA20 and GA25. Breed Science, 46(Suppl. 2), 70.

Park C H, Chen S, Shirsekar G, Zhou B, Khang C H, Songkumarn P, Afzal A J, Ning Y, Wang R, Bellizzi M,Valent B, Wang G L. 2012. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. The Plant Cell, 24, 4748–4762.

Park C H, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, Shi X, Ning Y, Zhou B, Suttiviriya P, Wang M, Umemura K, Wang G L. 2016. The E3 ligase APIP10 connects the effector AvrPiz-t to the NLR receptor Piz-t in rice. PLoS Pathogens, 12, e1005529.

Parker D, Beckmann M, Zubair H, Enot D P, Caracuel-Rios Z, Overy D P, Snowdon S, Talbot N J, Draper J. 2009. Metabolomic analysis reveals a common pattern of metabolic reprogramming during invasion of three host plant species by Magnaporthe grisea. The Plant Journal, 59, 723–737.

Pecenková T, Hála M, Kulich I, Kocourková D, Drdová E, Fendrych M, Toupalová H, Zársky V. 2011. The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. The Journal of Experimental Botany, 62, 2107–2116.

Qu S H, Liu G F, Zhou B, Bellizzi M, Zeng LR, Dai L Y, Han B, Wang G L. 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.

Ravensdale M, Bernoux M, Ve T, Kobe B, Thrall P H, Ellis J G, Dodds P N. 2012. Intramolecular interaction influences binding of the Flax L5 and L6 resistance proteins to their AvrL567 ligands. PLoS Pathogens, 8, e1003004.

Ray S, Singh P K, Gupta D K, Mahato A K, Sarkar C, Rathour R, Singh N K, Sharma T R. 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. Frontiers in Plant Science, 7, 1140.

Ribot C, Cesari S, Abidi I, Chalvon V, Bournaud C, Vallet J, Lebrun M, Morel J, Kroj T. 2013. The Magnaporthe oryzae effector AVR1-CO39 is translocated into rice cells independently of a fungal-derived machinery. The Plant Journal, 74, 1–12.

Sallaud C, Lorieux M, Roumen E, Tharreau D, Berruyer R, Svestasrani P, Notteghem J L. 2003. Identification of five new blast resistance genes in the highly blast-resistant rice variety IR64 using a QTL mapping strategy. Theoretical and Applied Genetics, 106 , 794–803.

Salmeron J, Oldroyd G, Rommens C, Scofield S, Kim H, Lavelle D, Dahlbeck D, Staskawicz B. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell, 86, 123–133.

Sarma G, Manning V, Ciuffetti L, Karplus P. 2005. Structure of Ptr ToxA: An RGD-containing host-selective toxin from Pyrenophora tritici-repentis. The Plant Cell, 17, 3190–3202.

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 genome wide comparison of paired nucleotide-binding site-leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics, 182, 1303–1311.

Sharma T R, Madhav M S, Singh B K, Shanker P, Jana T K, Dalal V, Pandit A, Singh A, Gaikwad K, Upreti H C, Singh N K. 2005. High-resolution mapping, cloning and molecular characterization of the Pi-kh gene of rice, which confers resistance to Magnaporthe grisea. Molecular Genetics and Genomics, 274, 569–578.

Sharma T R, Rai A K, Gupta S K, Singh N K. 2010. Broad-spectrum blast resistance gene Pi-kh cloned from rice line Tetep designated as Pi54. Journal of Plant Biochemistry and Biotechnology, 19, 87–89.

Singh R, Dangol S, Chen Y, Choi J, Cho Y S, Lee J E, Choi M O, Jwa N S. 2016. Magnaporthe oryzae effector AVR-Pii helps to establish compatibility by inhibition of the rice NADP-Malic enzyme resulting in disruption of oxidative burst and host innate immunity. Molecular Cells, 39, 426–438.

Skamnioti P, Gurr S J. 2009. Against the grain: Safeguarding rice from rice blast disease. Trends in Biotechnology, 27, 141–150.

Sone T, Takeuchi S, Miki S, Satoh Y, Ohtsuka K, Abe A, Asano K. 2013. Homologous recombination causes the spontaneous deletion of AVR-Pia in Magnaporthe oryzae. FEMS Microbiology Letters, 339, 102–109.

Stegmann M, Anderson R G, Ichimura K, Pecenkova T, Reuter P, ?ársky V, McDowell J M, Shirasu K, Trujillo M. 2012. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. The Plant Cell, 24, 4703–4716.

Stegmann M, Anderson R G, Westphal L, Rosahl S, McDowell J M, Trujillo M. 2013. The exocyst subunit Exo70B1 is involved in the immune response of Arabidopsis thaliana to different pathogens and cell death. Plant Signaling & Behavior, 8, e27421.

Su J, Wang W, Han J, Chen S, Wang C, Zeng L, Feng A, Yang J, Zhou B, Zhu X. 2015. Functional divergence of duplicated genes results in a novel blast resistance gene Pi50 at the Pi2/9 locus. Theoretical and Applied Genetics, 128, 2213–2225.

Sweigard J A, Carroll A M, Kang S, Farrall L, Chumley F G, Valent B. 1995. Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. The Plant Cell, 7, 1221–1233.

Takagi H, Uemura A, Yaegashi H, Tamiru M, Abe A, Mitsuoka C, Utsushi H, Natsume S, Kanzaki H, Matsumura H, Saitoh H, Yoshida K, Cano L M, 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 Phytologist, 200, 276–283.

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 Biology, 10, 175.

Tang M, Ning Y, Shu X, Dong B, Zhang H, Wu D, Wang H, Wang G L, Zhou B. 2017. The Nup98 homolog APIP12 targeted by the effector AvrPiz-t is involved in rice basal resistance against Magnaporthe oryzae. Rice, 10, 5.

Tang X, Frederick R, Zhou J, Halterman D, Jia Y, Martin G. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science, 274, 2060–2063.

Tanweer F, Rafii M, Sijam K, Rahim H, Ahmed F, Latif M. 2015. Current advance methods for the identification of blast resistance genes in rice. Comptes Rendus Biologies, 338, 321–334.

Tosa Y, Osue J, Eto Y, Oh H S, Nakayashiki H, Mayama S, Leong S A. 2005. Evolution of an avirulence gene, AVR1-CO39, concomitant with the evolution and differentiation of Magnaporthe oryzae. Molecular Plant-Microbe Interactions, 18, 1148–1160.

Trujillo M, Ichimura K, Casais C, Shirasu K. 2008. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Current Biology, 18, 1396–1401.

Wang C, Guncar G, Forwood J, Teh T, Catanzariti A, Lawrence G, Loughlin F, Mackay J, Schirra H, Anderson P, Ellis J, Dodds P, Kobe B. 2007. Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. The Plant Cell, 19, 2898–2912.

Wang J, Qu B, Dou S, Li L, Yin D, Pang Z, Zhou Z, Tian M, Liu G, Xie Q, Tang D, Chen X, Zhu L. 2015. The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biology, 15, 49.

Wang R, Ning Y, Shi X, He F, Zhang C, Fan J, Jiang N, Zhang Y, Zhang T, Hu Y, Bellizzi M, Wang G L. 2016. Immunity to rice blast disease by suppression of effector-triggered necrosis. Current Biology, 26, 2399–2411.

Wang Y, Pi L, Chen X, Chakrabarty P, Jiang J, DeLeon A, Liu G, Li L, Benny U, Oard J, Ronald, P, Song W. 2006. Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. The Plant Cell, 18, 3635–3646.

Wang Z, 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. The Plant Journal, 19, 55–64.

Williams S, Sohn K H, Wan L, Bernoux M, Sarris P, Segonzac C, Ve T, Ma Y, Saucet S, Ericsson D, Casey L, Lonhienne T, Winzor D, Zhang X, Coerdt A, Parker J, Dodds P, Kobe B, Jones J. 2014. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science, 344, 299–303.

Wu J, Fan Y, Li D, Zheng K, Leung H, Zhuang J. 2005. Genetic control of rice blast resistance in the durably resistant cultivar Gumei 2 against multiple isolates. Theoretical and Applied Genetics, 111, 50–56.

Wu J, Kou Y, Bao J, Li Y, Tang M, Zhu X, Ponaya A, Xiao G, Li J, Li C, Song M Y, Cumagun C J, Deng Q, Lu G, Jeon J S, Naqvi N I, Zhou B. 2015. Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytologist, 206, 1463–1475.

Wu W, Wang L, Zhang S, Li Z, Zhang Y, Lin F, Pan Q. 2014. Stepwise arms race between AvrPik and Pik alleles in the rice blast pathosystem. Molecular Plant-Microbe Interactions, 27, 759–769.

Xu X, Hayashi N, Wang C T, Fukuoka S, Kawasaki S, Takatsuji H, Jiang C J. 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. Molecular Breeding, 34, 691–700.

Yasuda N, Tsujimoto Noguchi M, Fujita Y. 2006. Partial mapping of avirulence genes AVR-Pii and AVR-Pia in the rice blast fungus Magnaporthe oryzae. Canadian Journal of Plant Pathology, 28, 494–498.

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. The Plant Cell, 21, 1573–1591.

Yuan B, Zhai C, Wang W J, Zeng X S, Xu X K, Hu H Q, Lin F, Wang L, Pan Q H. 2011. The Pik-p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes. Theoretical and Applied Genetics, 122, 1017–1028.

Zeng L R, Park C H, Venu R C, Gough J, Wang G L. 2008. Classification, expression pattern, and E3 ligase activity assay of rice U-box-containing proteins.Molecular Plant, 1, 800–815.

Zeng L R, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm B, Leung H, Wang G L. 2004. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. The Plant Cell, 16, 2795–2808.

Zhai C, Lin F, Dong Z Q, He X Y, Yuan B, Zeng X S, Wang L, Pan Q H. 2011. The isolation and characterization of Pik, a rice blast resistance gene which emerged after rice domestication. New Phytologist, 189, 321–334.

Zhai C, Zhang Y, Yao N, Lin F, Liu Z, Dong Z, Wang L, Pan Q. 2014. Function and interaction of the coupled genes responsible for Pik-h encoded rice blast resistance. PLoS ONE, 9, e98067.

Zhang S, Wang L, Wu W, He L, Yang X, Pan Q. 2015. Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib. Scientific Reports, 5, 11642.

Zhang Z, Zhang X, Zhou Z, Hu H, Liu M, Zhou B, Zhou J. 2013. Solution structure of the Magnaporthe oryzae avirulence protein AvrPiz-t. Journal of Biomolecular NMR, 55, 219–223.

Zhao T, Rui L, Li J, Nishimura M T, Vogel J P, Liu N, Liu S, Zhao Y, Dangl J L, Tang D. 2015. A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLoS Genetics, 11, e1004945.

Zhou B, Qu S H, Liu G F, Dolan M, Sakai H, Lu G D, Bellizzi M, Wang G L. 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. Molecular Plant-Microbe Interactions, 19, 1216–1228.

Zhu X, Chen S, Yang J, Zhou S, Zeng L, Han J, Su J, Wang L, Pan Q. 2012. The identification of Pi50(t), a new member of the rice blast resistance Pi2/Pi9 multigene family. Theoretical and Applied Genetics, 124, 1295–1304.