Purification and characterization of a novel hypersensitive response-inducing elicitor from magnaporthe oryzae that triggers defense response in rice

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Chen, Mingjia ^a   Zeng, Hongmei ^a   Qiu, Dewen ^a   Guo, Lihua ^a   Yang, Xiufen ^a   Shi, Huaixing ^a   Zhou, Tingting ^a   Zhao, Jing ^a  

^a AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID DERIVATIVE; COMPLEMENTARY DNA; FUNGAL PROTEIN; HYDROGEN PEROXIDE; HYPERSENSITIVE RESPONSE INDUCING PROTEIN ELICITOR; POLYPEPTIDE; PROTEIN MOHRIP1; UNCLASSIFIED DRUG; REACTIVE OXYGEN METABOLITE;

ALKALINITY; ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; ESCHERICHIA COLI; FUNGAL STRAIN; GENE EXPRESSION; GENETIC CODE; MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEFENSE; PLANT PATHOGEN INTERACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; RICE; SEEDLING; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TOBACCO; AMINO ACID SEQUENCE; CHEMISTRY; DNA SEQUENCE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; ISOLATION AND PURIFICATION; MAGNAPORTHE; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PLANT LEAF; POLYACRYLAMIDE GEL ELECTROPHORESIS; RESPIRATORY BURST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BACTERIA (MICROORGANISMS); MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE; NICOTIANA TABACUM;

AMINO ACID SEQUENCE; BASE SEQUENCE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; MAGNAPORTHE; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT LEAVES; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; RESPIRATORY BURST; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TOBACCO;

EID: 84862105502     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037654     Document Type: Article

References (71)

1. Panstruga R, Parker JE, Schulze-Lefert P, (2009) SnapShot: Plant immune response pathways. Cell 136: 978 e971-973.
2. Cui H, Xiang T, Zhou JM, (2009) Plant immunity: a lesson from pathogenic bacterial effector proteins. Cell Microbiol 11: 1453-1461.
3. Boller T, He SY, (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742-744.
4. Nürnberger T, Brunner F, (2002) Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Current Opinion in Plant Biology 5: 318-324.
5. Thomma BP, Nurnberger T, Joosten MH, (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4-15.
6. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
7. Katagiri F, Tsuda K, (2010) Understanding the plant immune system. Mol Plant Microbe Interact 23: 1531-1536.
8. Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, et al. (2006) Early Signaling Events Induced by Elicitors of Plant Defenses. Mol Plant Microbe Interact 19: 711-724.
9. Dixon RA, Harrison MJ, Lamb CJ, (1994) Early Events in the Activation of Plant Defense Responses. Annual Review of Phytopathology 32: 479-501.
10. Ebel J, Mithöfer A, (1998) Early events in the elicitation of plant defence. Planta 206: 335-348.
11. Yano A, Suzuki K, Uchimiya H, Shinshi H, (1998) Induction of Hypersensitive Cell Death by a Fungal Protein in Cultures of Tobacco Cells. Mol Plant Microbe Interact 11: 115-123.
12. Durrant WE, Dong X, (2004) Systemic acquired resistance. Annual Review of Phytopathology 42: 185-209.
13. Nürnberger T, (1999) Signal perception in plant pathogen defense. Cellular and Molecular Life Sciences 55: 167-182.
14. De Wit PJ, Mehrabi R, Van den Burg HA, Stergiopoulos I, (2009) Fungal effector proteins: past, present and future. Mol Plant Pathol 10: 735-747.
15. Ellis JG, Rafiqi M, Gan P, Chakrabarti A, Dodds PN, (2009) Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens. Current Opinion in Plant Biology 12: 399-405.
16. Bent AF, Mackey D, (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45: 399-436.
17. Hammond-Kosack KE, Parker JE, (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14: 177-193.
18. Zhao J, Davis LC, Verpoorte R, (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23: 283-333.
19. Apel K, Hirt H, (2004) Reactive Oxygen Species: Metabolism, Oxidative Stress, and Signal Transduction. Annual Review of Plant Biology 55: 373-399.
20. Bóka K, Orbán N, (2007) New Aspect of H2O2 Signaling. Plant Signaling & Behavior 2: 498-500.
21. Foyer CH, Noctor G, (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28: 1056-1071.
22. Wilson RA, Talbot NJ, (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7: 185-195.
23. Ribot C, Hirsch J, Balzergue S, Tharreau D, Nottéghem J-L, et al. (2008) Susceptibility of rice to the blast fungus, Magnaporthe grisea. Journal of Plant Physiology 165: 114-124.
24. Kanoh H, Haga M, Sekizawa Y, (1993) Transmembrane signalling operated at rice blade cells stimulated by blast fungus elicitor 2. Participation of calcium modulated protein. Journal of Pesticide Science 18: 325-332.
25. Schaffrath U, Scheinpflug H, Reisener HJ, (1995) An elicitor from Pyricularia oryzae induces resistance responses in rice: isolation, characterization and physiological properties. Physiological and Molecular Plant Pathology 46: 293-307.
26. Koga J, Yamauchi T, Shimura M, Ogawa N, Oshima K, et al. (1998) Cerebrosides A and C, Sphingolipid Elicitors of Hypersensitive Cell Death and Phytoalexin Accumulation in Rice Plants. Journal of Biological Chemistry 273: 31985-31991.
27. Qiu D, Mao J, Yang X, Zeng H, (2009) Expression of an elicitor-encoding gene from Magnaporthe grisea enhances resistance against blast disease in transgenic rice. Plant Cell Rep 28: 925-933.
28. Peng DH, Qiu DW, Ruan LF, Zhou CF, Sun M, (2011) Protein elicitor PemG1 from magnaporthe grisea induces systemic acquired resistance (SAR) in plants. Mol Plant Microbe Interact 24: 1239-1246.
29. Rep M, (2005) Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol Lett 253: 19-27.
30. Stuiver MH, Custers JH, (2001) Engineering disease resistance in plants. Nature 411: 865-868.
31. Dixon RA, (2001) Natural products and plant disease resistance. Nature 411: 843-847.
32. Lamb C, Dixon RA, (1997) The Oxidative Burst in Plant Disease Resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48: 251-275.
33. Levine A, Tenhaken R, Dixon R, Lamb C, (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583-593.
34. Jabs T, Dietrich RA, Dangl JL, (1996) Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide. Science 273: 1853-1856.
35. Alvarez MaE, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, et al. (1998) Reactive Oxygen Intermediates Mediate a Systemic Signal Network in the Establishment of Plant Immunity. Cell 92: 773-784.
36. Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC, (2008) Plant pathogenesis-related (PR) proteins: A focus on PR peptides. Plant Physiology and Biochemistry 46: 941-950.
37. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC, (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5: 308-316.
38. Kunkel BN, Brooks DM, (2002) Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5: 325-331.
39. Pieterse CMJ, van Loon LC, (1999) Salicylic acid-independent plant defence pathways. Trends in Plant Science 4: 52-58.
40. Turner JG, Ellis C, Devoto A, (2002) The Jasmonate Signal Pathway. The Plant Cell 14: S153-S164.
41. Mao J, Liu Q, Yang X, Long C, Zhao M, et al. (2010) Purification and expression of a protein elicitor from Alternaria tenuissima and elicitor-mediated defence responses in tobacco. Annals of Applied Biology 156: 411-420.
42. Zhang W, Yang X, Qiu D, Guo L, Zeng H, et al. (2011) PeaT1-induced systemic acquired resistance in tobacco follows salicylic acid-dependent pathway. Mol Biol Rep 38: 2549-2556.
43. Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, et al. (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257: 85-88.
44. Osman H, Mikes V, Milat ML, Ponchet M, Marion D, et al. (2001) Fatty acids bind to the fungal elicitor cryptogein and compete with sterols. FEBS Letters 489: 55-58.
45. Veit S, Worle JM, Nurnberger T, Koch W, Seitz HU, (2001) A novel protein elicitor (PaNie) from Pythium aphanidermatum induces multiple defense responses in carrot, Arabidopsis, and tobacco. Plant Physiol 127: 832-841.
46. Repka V, (2006) Early defence responses induced by two distinct elicitors derived from a Botrytis cinerea in grapevine leaves and cell suspensions. Biologia Plantarum 50: 94-106.
47. Mishra AK, Sharma K, Misra RS, (2009) Purification and characterization of elicitor protein from Phytophthora colocasiae and basic resistance in Colocasia esculenta. Microbiol Res 164: 688-693.
48. Wang B, Yang X, Zeng H, Liu H, Zhou T, et al. (2012) The purification and characterization of a novel hypersensitive-like response-inducing elicitor from Verticillium dahliae that induces resistance responses in tobacco. Applied Microbiology and Biotechnology 93: 191-201.
49. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B, (2009) Interaction Transcriptome Analysis Identifies Magnaporthe oryzae BAS1-4 as Biotrophy-Associated Secreted Proteins in Rice Blast Disease. The Plant Cell 21: 1273-1290.
50. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, et al. (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22: 1388-1403.
51. Dangl JL, Jones JDG, (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
52. Chisholm ST, Coaker G, Day B, Staskawicz BJ, (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
53. Liu J, Wang X, Mitchell T, Hu Y, Liu X, et al. (2010) Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. Mol Plant Pathol 11: 419-427.
54. Sauerborn J, Buschmann H, Ghiasi KG, Kogel KH, (2002) Benzothiadiazole Activates Resistance in Sunflower (Helianthus annuus) to the Root-Parasitic Weed Orobanche cuman. Phytopathology 92: 59-64.
55. Ahn IP, Kim S, Lee YH, (2005) Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol 138: 1505-1515.
56. Keller H, Blein JP, Bonnet P, Ricci P, (1996) Physiological and Molecular Characteristics of Elicitin-Induced Systemic Acquired Resistance in Tobacco. Plant Physiology 110: 365-376.
57. Gurr SJ, Rushton PJ, (2005) Engineering plants with increased disease resistance: what are we going to express? Trends in Biotechnology 23: 275-282.
58. Kim S, Park S-Y, Kim KS, Rho H-S, Chi M-H, et al. (2009) Homeobox Transcription Factors Are Required for Conidiation and Appressorium Development in the Rice Blast Fungus Magnaporthe oryzae. PLoS Genet 5: e1000757.
59. Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F, (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat Biotechnol 17: 282-286.
60. D'Silva I, Heath MC, (1997) Purification and characterization of two novel hypersensitive response-inducing specific elicitors produced by the cowpea rust fungus. J Biol Chem 272: 3924-3927.
61. Koch E, Slusarenko A, (1990) Arabidopsis Is Susceptible to Infection by a Downy Mildew Fungus. The Plant Cell 2: 437-445.
62. Li H, Xu H, Zhou Y, Zhang J, Long C, et al. (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315: 1000-1003.
63. Davis DA, Low PS, Heinstein P, (1998) Purification of a glycoprotein elicitor of phytoalexin formation fromVerticillium dahliae. Physiological and Molecular Plant Pathology 52: 259-273.
64. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB, (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal 11: 1187-1194.
65. Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, et al. (1997) Early Events Induced by the Elicitor Cryptogein in Tobacco Cells: Involvement of a Plasma Membrane NADPH Oxidase and Activation of Glycolysis and the Pentose Phosphate Pathway. The Plant Cell Online 9: 2077-2091.
66. Gómez-Gómez L, Felix G, Boller T, (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. The Plant Journal 18: 277-284.
67. Brault M, Amiar Z, Pennarun A-M, Monestiez M, Zhang Z, et al. (2004) Plasma Membrane Depolarization Induced by Abscisic Acid in Arabidopsis Suspension Cells Involves Reduction of Proton Pumping in Addition to Anion Channel Activation, Which Are Both Ca2+ Dependent. Plant Physiology 135: 231-243.
68. Nishizawa Y, Nishio Z, Nakazono K, Soma M, Nakajima E, et al. (1999) Enhanced resistance to blast (Magnaporthe grisea) in transgenic Japonica rice by constitutive expression of rice chitinase. TAG Theoretical and Applied Genetics 99: 383-390.
69. Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, et al. (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Molecular Genetics and Genomics 279: 415-427.
70. Hwang S-H, Lee I, Yie S, Hwang D-J, (2008) Identification of an OsPR10a promoter region responsive to salicylic acid. Planta 227: 1141-1150.
71. Xie XZ, Xue YJ, Zhou JJ, Zhang B, Chang H, et al. (2011) Phytochromes regulate SA and JA signaling pathways in rice and are required for developmentally controlled resistance to Magnaporthe grisea. Mol Plant 4: 688-696.