Recent Progress of Interactions between Rice and Pathogens

doi:10.11924/j.issn.1000-6850.2014-2012

Abstract

Abstract: Rice blast and blight, caused by the fungal pathogen Magnaporthe oryzae (M. oryzae) and the bacterial pathogen Xanthomonas oryzae pv. oryzae (Xoo) respectively, are the most destructive diseases of rice in the world. The interactions between rice-M. oryzae and rice-Xoo have become model systems in the study of plant- pathogen interactions. In this review, the author summarized recent research on the structure and function of isolated resistance genes to M. oryzae and Xoo, a number of novel identified pathogen-associated molecular patterns (PAMPs) and effectors related to M. oryzae and Xoo, and PAMP- and effector-triggered rice immunity responses and signaling transduction mediated by M. oryzae or Xoo, suggesting that the interactions between avirulence effectors and their cognate resistance proteins could provide new insights into the molecular basis of plant-pathogen interactions, especially useful for rice breeding against M. oryzae and Xoo.

References

[1] Dai L Y, Liu X L, Xiao Y H, et al. Recent Advances in Cloning and Characterization of Disease Resistance Genes in Rice[J]. J Integr Plant Biol,2007,49(1):112-119.
[2] Ausubel F M. Are innate immune signaling pathways in plants and animals conserved[J]. Nat Immunol,2005,6(10):973-979.
[3] Nürnberger T, Brunner F, Kemmerling B, et al. Innate immunity in plants and animals: striking similarities andobvious differences[J]. Immunol Rev,2004,198(1):249-266.
[4] Flor H H: Inheritance of pathogenicity in Melampsora lini[J]. Phytopathology,1942,32:653-669.
[5] Song W Y, Wang G L, Chen L L, et al. A receptor kinase- like protein encoded by the rice disease resistance gene, Xa21[J]. Science,1995,270(5243):1804-1806.
[6] He C, javascript: popRef ('a1') Fong S H, javascript: popRef ('a1') Yang D, et al. BWMK1, a Novel MAP Kinase Induced by Fungal Infection and Mechanical Wounding in Rice[J]. Mol Plant Microbe Interact,1999,12(12):1064-1073.
[7] Zeng L, Yin Z, Chen J, et al. Fine genetic mapping and physical delimitation of the lesion mimic gene Spl11 to a 160- kb DNA segment of the rice genome[J]. Molecular Genet Genomics,2002, 268(2):253-261.
[8] Liu J, Li W, Ning Y, et al. The U-Box E3 Ligase SPL11/PUB13 Is a Convergence Point of Defense and Flowering Signaling in Plants [J]. Plant Physiol,2012,160(1):28-37.
[9] Qu S, Liu G, Zhou B, et al. 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[J]. Genetics, 2006,172(3):1901-1914.
[10] Dai L, Wu J, Li X, et al. Genomic structure and evolution of the Pi2/ 9 locus in wild rice species[J]. Theor Appl Genet,2010,121(2):295- 309.
[11] Zhou B, Qu S, Liu G, et al. The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea[J]. Mol Plant Microbe Interact,2006,19(11):1216-1228.
[12] Li W, Wang B, Wu J, et al. 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[J]. Mol Plant Microbe Interact,2009,22(4):411-420.
[13] Liu X, Lin F, Wang L, et al. 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[J]. Genetics,2007,176(4):2541-2549.
[14] Lin F, Chen S, Que Z, et al. 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[J]. Genetics,2007,177(3):1871-1880.
[15] Hua L, Wu J, Chen C, et al. The isolation of Pi1, an allele at the Pik locus which confers broad spectrum resistance to rice blast[J]. Theor Appl Genet,2012,125(5):1047-1055.
[16] Sun X, Cao Y, Yang Z , et al. Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein[J]. Plant J,2004,37(4):517-527.
[17] Cao Y, Duan L, Li H, et al. Functional analysis of Xa3/Xa26 family members in rice resistance to Xanthomonas oryzae pv. oryzae[J]. Theor Appl Genet,2007,115(7):887-895.
[18] Gu K, Yang B, Tian D, et al. R gene expression induced by a typeIII effector triggers disease resistance in rice[J]. Nature,2005,435 (7045):1122-1125.
[19] Yang B, Sugio A, White F F. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice[J]. Proc Natl Acad Sci U S A,2006, 103(27):10503-10508.
[20] Guo M, Chen Y, Du Y, et al. The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae[J]. PLoS Pathog,2011,7(2):e1001302.
[21] Yan X, Li Y, Yue X, et al. Two Novel Transcriptional Regulators Are Essential for Infection- related Morphogenesis and Pathogenicity of the Rice Blast Fungus Magnaporthe oryzae[J]. PLoS Pathog,2011,7(12):e1002385.
[22] Feng F, Fan Yang F, Rong W, et al. A Xanthomonas uridine 5'- monophosphate transferase inhibits plant immune kinases[J].Nature, 2012,485(7396):114-118.
[23] Liu W, Liu J, Triplett L, et al. Novel Insights into Rice Innate Immunity against Bacterial and Fungal Pathogens[J]. Annu Rev Phytopathol,2014,52:213-241.
[24] Gregory T B, Wu K S, Farrall L, et al. A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta[J]. Plant Cell,2000,12(11):2033-2045.
[25] Orbach M J, Farrall L, Sweigard J A, et al. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta[J]. Plant Cell,2000,12(11):2019-2032.
[26] Wang Z X, Yano M, Yamanouchi U, et al. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes[J]. Plant J,1999,19(1): 55-64.
[27] Ashikawa K, Hayashi N, Yamane H, et al. Two adjacent nucleotidebinding site-leucine-rich repeat class genes are required to confer Pikm- specific rice blast resistance[J]. Genetics,2008,180(4):2267- 2276.
[28] Yoshida K, Saitoh H, Fujisawa S, et al. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae[J]. Plant Cell,2009,21(5):1573-1591.
[29] Hayashi K, Yoshida H. Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter[J]. Plant J,2009,57(3):413-425.
[30] Kawano Y, Akamatsu A, Hayashi K. Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity[J]. Cell Host Microbe,2010,7(5):362-375.
[31] Shang J, Tao Y, Chen X, et al. 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[J]. Genetics,2009,182(4):1303-1311.
[32] Lee S K, Song M Y, Seo Y S, et al. Rice Pi5-mediated resistance to Magnaporthe oryzae requires the presence of two coiled- coilnucleotide-binding-leucine-rich repeat genes[J]. Genetics,2009,181 (4):1627-1638.
[33] Sharma T R, Rai A K, Gupta S K, et al. Broad- spectrum blast resistance gene Pi-kh cloned from rice line tetep designated as Pi54 [J]. J Plant Biochem Biotechnol,2010,19(1):87-89.
[34] Takahashi A, Hayashi N, Miyao A, et al. Unique features of the rice blast resistance Pish locus revealed by large scale retrotransposontagging[J]. BMC Plant Biol,2010,10:175.
[35] Hayashi N, Inoue H, Kato T, et al. Durable panicle blast-resistance gene Pb1 encodes an atypical CC- NBS- LRR protein and was generated by acquiring a promoter through local genome duplication [J]. Plant J,2010,64(3):498-510.
[36] Okuyama Y, Kanzaki H, Abe A, et al. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes[J]. Plant J,2011, 66(3):467-479.
[37] Yuan B, Zhai C, Wang W, et al. The Pik- p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes[J]. Theor Appl Genet,2011,122(5):1017-1028.
[38] Zhai C, Lin F, Dong Z, et al. The isolation and characterization of Pik, a rice blast resistance gene which emerged after rice domestication[J]. New Phytol,2011,189(1):321-334.
[39] Chen J, Shi Y, Liu W, et al. A Pid3 allele from rice cultivar Gumei2 confers resistance to Magnaporthe Oryzae[J]. J Genet Genomics, 2011,38(5):209-216.
[40] Fukuoka S, Yamamoto S- I, Mizobuchi R. Multiple functional polymorphisms in a single disease resistance gene in rice enhance durable resistance to blast[J]. Sci Rep,2014,4:4550.
[41] Ribot C, Cesari S, Abidi I, et al. The Magnaporthe oryzae effector AVR1- CO39 is translocated into rice cells independently of a fungal-derived machinery[J]. Plant J,2013,74(1):1-12.
[42] Yoshimura S, Yamanouchi U, Katayose Y, et al. Expression of Xa1, a bacterial blight- resistance gene in rice, is induced by bacterial inoculation[J]. Proc Natl Acad Sci U S A,1998,95(4):1663-1668.
[43] Chen X, Shang J, Chen D, et al. A B-lectin receptor kinase gene conferring rice blast resistance[J]. Plant J,2006,46(5):794-804.
[44] Fukuoka S, Saka N, Koga H, et al. Loss of function of a prolinecontaining protein confers durable disease resistance in rice[J]. Science, 2009,325(5943):998-1001.
[45] Iyer A S, McCouch S R. The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance[J]. Mol Plant Microbe Interact, 2004,17(12):1348-1354.
[46] Chen L Q, Hou B H, Lalonde S, et al. Sugar transporters for intercellular exchange and nutrition of pathogens[J]. Nature,2010, 468(7323):527-532.
[47] R?mer P, Recht S, Strauss T, et al. Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae[J]. New Phytol,2010,187(4):1048-1057.
[48] Yu Y, Streubel J, Balzergue S, et al. Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene[J]. Mol Plant Microbe Interact,2011,24(9):1102-1113.
[49] Streubel J, Pesce C, Hutin M, et al. Five phylogenetically close rice SWEET genes confer TAL effector- mediated susceptibility to Xanthomonas oryzae pv. oryzae[J]. New Phytol,2013,200(3):808- 819.
[50] Liu Q, Yuan M, Zhou Y, et al. A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice[J]. Plant Cell Environ,2011,34(11):1958-1969.
[51] Tian D, Wang J, Zeng X, et al. The rice TAL effector- dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum[J]. Plant Cell,2014,26(1):497-515.
[52] Bohnert H U, Fudal I, Dioh W, et al. A putative polyketide synthase/ peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice[J]. Plant Cell,2004,16(9):2499-2513.
[53] Kang S, Sweigard J A, Valent B, et al. The PWL host specificity gene family in the blast fungus Magnaporthe grisea[J]. Mol Plant Microbe Interact,1995,8(6):939-948.
[54] Sweigard J A, Carroll A M, Kang S, et al. Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus[J]. Plant Cell,1995,7(8):1221-1233.
[55] Albar L, Bangratz-Reyser M, Hébrard E, et al. Mutations in the eIF (iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus[J]. Plant J,2006,47(3):417-426.
[56] Du B, Zhang W, Liu B, et al. Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice[J]. Proc Natl Acad Sci U S A,2009,106(52):22163-22168.
[57] Chen X W, Ronald P C. Innate immunity in rice[J]. Trends Plant Sci, 2011,16(8):451-459.
[58] Kaku H, Nishizawa Y, Ishii-Minami N, et al. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor[J]. Proc Natl Acad Sci USA,2006,103(29):11086-11091.
[59] Che F S, Nakajima Y, Tanaka N, et al. Flagellin from an incompatible strain of Pseudomonas avenae induces a resistance response in cultured rice cells[J]. J Biol Chem,2000,275(41):32347- 32356.
[60] Desaki Y, Miya A, Venkatesh B, et al. Bacterial lipopolysaccharides induce defense responses associated with programmed cell death in rice cells[J]. Plant Cell Physiol,2006,47(11):1530-1540.
[61] Park C J, Han S W, Chen X, et al. Elucidation of XA21-mediated innate immunity[J]. Cell Microbiol,2010,12(18):1017-1025.
[62] Park C J, Peng Y, Chen X, et al. Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21- mediated innate immunity[J]. PLoS Biol,2008,6(9),1910-1926.
[63] Park C J, Ronald P C. Cleavage and nuclear localization of the rice XA21 immune receptor[J]. Nat Commun,2012,3(6):920.
[64] Park C J, Bart R, Chern M, et al. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21- mediated innate immunity in rice[J]. PLoS One,2010,5(2):e9262.
[65] Wang Y S, Pi L Y, Chen X, et al. Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance [J]. Plant Cell,2006,18(12):3635-3646.
[66] Wang G L, Ruan D L, Song W Y, et al. Xa21D encodes a receptorlike molecule with a leucine- rich repeat domain that determines race- specific recognition and is subject to adaptive evolution[J]. Plant Cell,1998,10(5):765-780.
[67] Yamaguchi T, Tanabe S, Minami E, et al. Activation of phospholipase D induced by hydrogen peroxide in suspensioncultured rice cells[J]. Plant Cell Physiol,2004,45(9):1261-1270.
[68] Yamaguchi T, Minami E, Ueki J, et al. Elicitor- induced activation of phospholipases plays an important role for the induction of defense responses in suspension- cultured rice cells[J]. Plant Cell Physiol,2005,46(4):579-587.
[69] Mentlak T A, Kombrink A, Shinya T, et al. Effector- mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease[J]. Plant Cell,2012,24(1):322-335.
[70] Chen L T, Hamada S, Fujiwara M, et al. The Hop/Sti1- Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity[J]. Cell Host Microbe,2010, 7(3):185-196.
[71] Shimizu T, Nakano T, Takamizawa D, et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice[J]. Plant J,2010,64(2):204-214.
[72] Kishimoto K, Kouzai Y, Kaku H, et al. Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice[J]. Plant J,2010,64(2):343-354.
[73] Gómez- Gómez L, Boller T. FLS2: an LRR receptor- like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis[J]. Mol Cell,2000,5(6):1003-1011.
[74] Sun W, Cao Y, Jansen Labby K, et al. Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function[J]. The Plant Cell,2012,24(3): 1096-1113.
[75] Lu D, Lin W, Gao X, et al. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity[J]. Science,2011,332(6036):1439-1442.
[76] Liu B, Li J F, Ao Y, et al. Lysin motif–containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity[J]. Plant Cell,2012,24(8):3406-3419.
[77] Jia Y, McAdams S A, Bryan G T, et al. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance[J]. EMBO J, 2000,19(15):4004-4014.
[78] Jia Y, Martin R. Identification of a new locus, Ptr(t), required for rice blast resistance gene Pi- ta mediated resistance[J]. Mol Plant Microbe Interact,2008,21(4):396-403.
[79] Park C H, Chen S, Shirsekar G, et al. The Magnaporthe oryzae effector AvrPiz- t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice[J]. Plant Cell,2012,24(11):4748-4762.
[80] Kanzaki H, Yoshida K, Saitoh H, et al. Arms race co-evolution of Magnaporthe oryzae AVR- Pik and rice Pik genes driven by their physical interactions[J]. Plant J, 2012,72(6):894-907.
[81] Mosquera G, Giraldo M C, Khang CH, et al. Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1- 4 as Biotrophy-associated secreted proteins in rice blast disease[J]. Plant Cell,2009,21(4):1273-1290.
[82] Saitoh H, Fujisawa S, Mitsuoka C, et al. Large- scale gene disruption in Magnaporthe oryzae identifies MC69, a secreted protein required for infection by monocot and dicot fungal pathogens[J]. PLoS Pathog,2012,8(5):e1002711.
[83] Jiang G H, Xia Z H, Zhou Y L, et al. Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAgamma1 [J]. Mol Genet Genomics,2006,275(4):354-366.
[84] Antony G, Zhou J, Huang S, et al. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3[J]. Plant Cell,2010,22(11):3864-3876.
[85] Moscou M J, Bogdanove A J. A simple cipher governs DNA recognition by TAL effectors[J]. Science,2009,326(5959):1501.
[86] Gu K, Tian D, Qiu C, et al. Transcription activator- like type III effector AvrXa27 depends on OsTFIIAgamma5 for the activation of Xa27 transcription in rice that triggers disease resistance to Xanthomonas oryzae pv. oryzae[J]. Mol Plant Pathol,2009,10(6): 829-835.
[87] Yuan M, Chu Z, Li X, et al. The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution[J]. Plant Cell,2010,22(9):3164-3176.
[88] Manosalva P M, Davidson R M, Liu B, et al. A germin-like protein gene family functions as a complex quantitative trait locus conferring broad- spectrum disease resistance in rice[J]. Plant Physiol,2009,149(1):286-296.
[89] Yang Z, Fu Y. ROP/RAC GTPase signaling[J]. Curr Opin Plant Biol,2007,10(5):490-494.
[90] Yang Z. Small GTPases: versatile signaling switches in plants[J]. Plant Cell,2002,14(Supplement):S375-388.
[91] Miki D, Itoh R, Shimamoto K, et al. RNA silencing of single and multiple members in a gene family of rice[J]. Plant Physiol,2005, 138(4):1903-1913.
[92] Ono E, Wong H L, Kawasaki T, et al. Essential role of the small GTPase Rac in disease resistance of rice[J]. Proc Natl Acad Sci U S A,2001,98(2):759-764.
[93] Suharsono U, Fujisawa Y, Kawasaki T, et al. The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice[J]. Proc Natl Acad Sci U S A,2002,99(20): 13307-13312.
[94] Akamatsu A, Wong H L, Fujiwara M, et al. An OsCEBiP/ OsCERK1- OsRacGEF1- OsRac1 module is an essential early component of chitin-induced rice immunity[J]. Cell Host Microbe, 2013,13(4):465-476.
[95] Wong H L, Pinontoan R, Hayashi K, et al. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N- terminal extension[J]. Plant Cell,2007,19(12):4022-4034.
[96] Nakashima A, Chen L, Thao N P, et al. RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex[J]. Plant Cell,2008,20(8):2265-2279.
[97] Lieberherr D, Thao N P, Nakashima A, et al. A sphingolipid elicitorinducible mitogen-activated protein kinase is regulated by the small GTPase OsRac1 and heterotrimeric G- protein in rice 1[J]. Plant Physiol,2005,138(3):1644-1652.
[98] Kawasaki T, Henmi K, Ono E, et al. The small GTP-binding protein Rac is a regulator of cell death in plants[J]. Proc Natl Acad Sci U S A,1999,96(19):10922-10926.
[99] Zhang S, Klessig D F. MAPK cascades in plant defense signaling [J]. Trends Plant Sci,2001,6(11):520-527.
[100] Seo Y S, Chern M, Bartley L E, et al. Towards establishment of a rice stress response interactome[J]. PLoS Genet,2011,7(4): e1002020.
[101] Kishi- Kaboshi M, Takahashi A, Hirochika H. MAMP- responsive MAPK cascades regulate phytoalexin biosynthesis[J]. Plant Signal Behav,2010,5(12):1653-1656.
[102] Pandey S P, Somssich I E. The role of WRKY transcription factors in plant immunity[J]. Plant Physiol,2009,150(4):1648-1655.
[103] Peng Y, Barhley L E, Chen X, et al. OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice[J]. Mol Plant,2008,1(3):446-458.
[104] Peng Y, Bartley L E, Canlas P, et al. OsWRKY IIa transcription factors modulate rice innate immunity[J]. Rice,2010,3(1):36-42.
[105] Wang H, Hao J, Chen X, et al. Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants [J]. Plant Mol Biol,2007,65(6):799-815.
[106] Fitzgerald H A, Canlas P E, Chern M S, et al. Alteration of TGA factor activity in rice results in enhanced tolerance to Xanthomonas oryzae pv. oryzae[J]. Plant J,2005,43(3):335-347.
[107] Nakashita H, Yasuda M, Nitta T, et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice[J]. Plant J, 2003,33(5):887-898.
[108] Mei C, Qi M, Sheng G, et al. Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection [J]. Mol Plant Microbe Interact,2006,19(10):1127-1137.
[109] Jiang C J, Shimono M, Sugano S, et al. Abscisic acid interacts antagonistically with salicylic acid signaling pathway in riceMagnaporthe grisea interaction[J]. Mol Plant Microbe Interact, 2010,23(6):791-798.
[110] Dean R A, Talbot N J, Ebbole D J, et al. The genome sequence of the rice blast fungus Magnaporthe grisea[J]. Nature,2005,434 (7036):980-986.
[111] Mitsuhara I, Iwai T, Seo S, et al. Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense- related signal compounds [J]. Mol Genet Genomics, 2008,279(4):415-427.
[112] Park C H, Kim S, Park J Y, et al. Molecular characterization of a pathogenesis-related protein 8 gene encoding a class III chitinase in rice[J]. Mol Cells,2004,17(1):144-150.
[113] Kim S T, Yu S, Kang Y H, et al. The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity[J]. Plant Cell Rep,2008,27(3):593-603.