In-depth insight into in vivo apoplastic secretome of rice-Magnaporthe oryzae interaction

Journal of Proteomics

Volumn 78, Issue , 2013, Pages 58-71

  Kim, Sang Gon ^a   Wang, Yiming ^a   Lee, Kyung Hee ^a   Park, Zee Yong ^b   Park, Jongsun ^c   Wu, Jingni ^a   Kwon, Soon Jae ^d   Lee, Yong Hwan ^c   Agrawal, Ganesh Kumar ^e   Rakwal, Randeep ^e,f,g   Kim, Sun Tae ^d   Kang, Kyu Young ^a  

^a Gyeongsang National University   (South Korea)

^b Gwangju Institute of Science and Technology (GIST)   (South Korea)

^c Seoul National University   (South Korea)

^d Pusan National University   (South Korea)

^e Research Laboratory for Biotechnology and Biochemistry RLABB   (Nepal)

^f UNIVERSITY OF TSUKUBA   (Japan)

^g SHOWA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

2 DGE; In vivo apoplastic proteome; Magnaporthe oryzae; MudPIT; Secretome

Indexed keywords

ANTIOXIDANT; APOPLASTIC SECRETOME; GLYCOSIDASE; PEPTIDASE; PROTEINASE; REACTIVE OXYGEN METABOLITE; SECRETORY PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CELL WALL HYDROLYSIS; CELLULAR STRESS RESPONSE; ENERGY METABOLISM; EXTRACTION; GENE EXPRESSION PROFILING; HOST PATHOGEN INTERACTION; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; INOCULATION; MAGNAPORTHE ORYZAE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE;

FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; MAGNAPORTHE; ORYZA SATIVA; OXIDATIVE STRESS; PLANT DISEASES; PLANT PROTEINS; PROTEOME;

MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE;

EID: 84870707963     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.10.029     Document Type: Article

References (74)

1. Liu J., Wang X., Mitchell T., Hu Y., Liu X., Dai L., et al. Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. Mol Plant Pathol 2010, 11:419-427.
2. Talbot N.J. On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 2003, 57:177-202.
3. Kawasaki S. Proceedings of the 3rd International Rice Blast Conference. Rice Blast: Interaction with Rice and Control 2004, Kluwer Academic Publishers, Dordrecht, The Netherlands.
4. Dean R.A., Talbot N.J., Ebbole D.J., Farman M.L., Mitchell T.K., Orbach M.J., et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
5. Goff S.A., Ricke D., Lan T.H., Presting G., Wang R., Dunn M., et al. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 2002, 296:92-100.
6. International Rice Genome Sequencing Project The map based sequence of the rice genome. Nature 2005, 436:793-800.
7. Yu J., Hu S., Wang J., Wong G.K., Li S., Liu B., et al. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 2002, 296:79-92.
8. Chen L.J., Lee D.S., Song Z.P., Suh H.S., Lu B.R. Gene flow from cultivated rice (Oryza sativa) to its weedy and wild relatives. Ann Bot 2004, 93:67-73.
9. Bajaj S., Mohanty A. Recent advances in rice biotechnology-towards genetically superior transgenic rice. Plant Biotechnol J 2005, 3:275-307.
10. Krishnan A., Guiderdoni E., An G., Hsing Y.I., Han C.D., Lee M.C., et al. Mutant Resources in Rice for Functional Genomics of the Grasses. Plant Physiol 2009, 149:165-170.
11. Meng Y., Patel G., Heist M., Betts M.F., Tucker S.L., Galadima N., et al. A systematic analysis of T-DNA insertion events in Magnaporthe oryzae. Fungal Genet Biol 2007, 44:1050-1064.
12. Agrawal G.K., Rakwal R. Rice proteomics: A cornerstone for cereal food crop proteomes. Mass Spectrom Rev 2006, 25:1-53.
13. Agrawal G.K., Jwa N.S., Lebrun M.H., Job D., Rakwal R. Plant secretome: unlocking secrets of the secreted proteins. Proteomics 2010, 10:799-827.
14. Ebbole D.J. Magnaporthe as a model for understanding host-pathogen interactions. Annu Rev Phytopathol 2007, 45:437-456.
15. Valent B., Khang C.H. Recent advances in rice blast effector research. Curr Opin Plant Biol 2010, 13:434-441.
16. Kim S.G., Kim S.T., Kim S.K., Kang K.Y. Gene expression profiling in rice infected with rice blast fungus using SAGE. Plant Pathol J 2008, 24:384-391.
17. Li Q., Chen F., Sun L., Zhang Z., Yang Y., He Z. Expression profiling of rice genes in early defense responses to blast and bacterial blight pathogens using cDNA microarray. Physiol Mol Plant Pathol 2006, 68:51-60.
18. Mathioni S.M., Beló A., Rizzo C.J., Dean R.A., Donofrio N.M. Transcriptome profiling of the rice blast fungus during invasive plant infection and in vitro stresses. BMC Genomics 2011, 12:49.
19. Agrawal G.K., Rakwal R. Rice proteomics: A move toward expanded proteome coverage to comparative and functional proteomics uncovers the mysteries of rice and plant biology. Proteomics 2011, 11:1630-1649.
20. Jones O.A.H., Maguire M.L., Griffin J.L., Jung H.Y., Shibato S., Rakwal R., et al. Using metabolic profiling to assess plant-pathogen interactions: an example using rice (Oryza sativa) and the blast pathogen Magnaporthe grisea. Eur J Plant Pathol 2011, 129:539-554.
21. Kamoun S. A catalogue of the effector sectretome of plant pathogenic oomycetes. Annu Rev Phytopathol 2006, 44:41-60.
22. Stergiopoulos I., De Wit P.J.G.M. Fungal effector proteins. Annu Rev Phytopathol 2009, 47:233-263.
23. Agrawal G.K., Rakwal R. Plant Proteomics: Technologies, Strategies, and Applications 2008, John Wiley & Sons, Inc., Hoboken, NJ, USA. G.K. Agrawal, R. Rakwal (Eds.).
24. Thiellement H., Zivy M., Damerval C., Mechin V. Plant Proteomics: Methods and Protocols 2007, vol. 355. Humana Press.
25. Kim S.T., Kang Y.H., Wang Y., Wu J., Park Z.Y., Rakwal R., et al. Secretome analysis of differentially induced proteins in rice suspension-cultured cells triggered by rice blast fungus and elicitor. Proteomics 2009, 9:1302-1313.
26. Kim S.T., Kim S.G., Hwang D.H., Kang S.Y., Kim H.J., Lee B.H., et al. Proteomic analysis of pathogen-responsive proteins from rice leaves induced by rice blast fungus, Magnaporthe grisea. Proteomics 2004, 4:3569-3578.
27. Donofrio N.M., Oh Y., Lundy R., Pan H., Brown D.E., Jeong J.S., et al. Global gene expression during nitrogen starvation in the rice blast fungus, Magnaporthe grisea. Fungal Genet Biol 2006, 43:605-617.
28. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
29. Chen X., Kim S.T., Cho W.K., Rim Y., Kim S., Kim S.W., et al. Proteomics of weakly bound cell wall proteins in rice calli. J Plant Physiol 2008, 166:675-685.
30. Kim H., Jo S., Song H.J., Park Z.Y., Park C.S. Myelin basic protein as a binding partner and calmodulin adaptor for the BKCa channel. Proteomics 2007, 7:2591-2602.
31. Choi J., Park J., Kim D., Jung K., Kang S., Lee Y. Fungal Secretome Database: Integrated platform for annotation of fungal secretomes. BMC Genomics 2010, 11:105.
32. Horton P., Park K.J., Obayashi T., Fujita N., Harada H., Adams-Collier C.J., et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res 2007, 35:W585-W587.
33. Emanuelsson O. Predicting protein subcellular localization from amino acid sequence information. Brief Bioinform 2002, 3:361-376.
34. Sambrook J., Russell D.W. Molecular Cloning, A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York.
35. Terry M., Bonner B. An examination of centrifugation as a method of extracting an extracellular solution from peas, and its use for the study of indole acetic acid-induced growth. Plant Physiol 1980, 66:321-325.
36. Jung Y.H., Jeong S.H., Kim S.H., Singh R., Lee J.E., Cho Y.S., et al. Systematic secretome analyses of rice leaf and seed callus suspension-cultured cells: workflow development and establishment of high-density two-dimensional gel reference maps. J Proteome Res 2008, 7:5187-5210.
37. Bayer E.M., Bottrill A.R., Walshaw J., Vigouroux M., Naldrett M.J., Thomas C.L., et al. Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 2006, 6:301-311.
38. Kim S.T., Cho K.S., Yu S., Kim S.G., Hong J.C., Han C.D., et al. Proteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells. Proteomics 2003, 3:2368-2378.
39. Nickel W., Seedorf M. Unconventional mechanisms of protein transport to the cell surface of eukaryotic cells. Annu Rev Cell Dev Biol 2008, 24:287-308.
40. Nickel W., Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009, 10:148-155.
41. Hückelhoven R. Transport and secretion in plant-microbe interactions. Curr Opin Plant Biol 2007, 10:573-579.
42. Lippincott-Schwartz J., Yuan L.C., Bonifacino J.S., Klausner R.D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 1989, 56:801-813.
43. Shenton M.R., Berberich T., Kamo M., Yamashita T., Taira H., Terauchi R. Use of interacellular washing fluid to investigate the secreted proteome of the rice-Magnaphorthe interaction. J Plant Res 2012, 125:311-316.
44. Shah P., Powell A.L., Orlando R., Bergmann C., Gutierrez-Sanchez G. Proteomic analysis of ripening tomato fruit infected by Botrytis cinerea. J Proteome Res 2012, 11:2178-2192.
45. Wingler A., Purdy S., MacLean J.A., Pourtau N. The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 2006, 57:391-399.
46. Zagrobelny M., Bak S., Rasmussen A.V., Jorgensen B., Naumann C.M., Moller B.L. Cyanogenic glucosides and plant-insect interactions. Phytochemistry 2004, 65:293-306.
47. Jamet E., Canut H., Boudart G., Pont-Lezica R.F. Cell wall proteins: a new insight through proteomics. Trends Plant Sci 2006, 11:33-39.
48. Minic Z. Physiological roles of plant glycoside hydrolases. Planta 2008, 227:723-740.
49. Hückelhoven R. Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 2007, 45:101-127.
50. Rahme G.L., Mindrinos M.N., Panopoulos N.J. Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. J Bacteriol 1992, 174:3499-3507.
51. Schulte R., Bonas U. A Xanthomonas pathogenicity locus is induced by sucrose and sulphur-containing amino acids. Plant Cell 1992, 4:79-86.
52. Kim S., Park J., Park S.Y., Mitchell T.K., Lee Y.H. Identification and analysis of in planta expressed genes of Magnaporthe oryzae. BMC Genomics 2010, 11:104.
53. Wilson D.B. Three microbial strategies for plant cell wall degradation. Ann N Y Acad Sci 2008, 1125:289-297.
54. Schaller A. A cut above the rest: the regulatory function of plant proteases. Planta 2004, 220:183-197.
55. Beers E.P., Woffenden B.J., Zhao C. Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol Biol 2000, 44:399-415.
56. Fowler J.H., Narváez-Vásquez J., Aromdee D.N., Pautot V., Holzer F.M., Walling L.L. Leucine aminopeptidase regulates defense and wound signaling in tomato downstream of jasmonic acid. Plant Cell 2009, 21:1239-1251.
57. Xia Y., Suzuki H., Borevitz J., Blount J., Guo Z., Patel K., et al. An extracellular aspartic protease functions in Arabidopsis disease signaling. EMBO J 2004, 223:980-988.
58. Meichtry J., Amrhein N., Schaller A. Charazterization of the subtilase gene family in tomato (Lycopersicon esculentum Mill). Plant Mol Biol 1999, 39:749-760.
59. Brown S.H., Yarden O., Gollop N., Chen S., Zveibil A., Belausov E., et al. Differential protein expression in Colletotrichum acutatum: changes associated with reactive oxygen species and nitrogen starvation implicated in pathogenicity on strawberry. Mol Plant Pathol 2008, 9:171-190.
60. Donofrio N.M., Oh Y., Lundy R., Pan H., Brown D.E., Jeong J.S., et al. Global gene expression during nitrogen starvation in the rice blast fungus, Magnaporthe grisea. Fungal Genet Biol 2006, 43:605-617.
61. Saitoh H., Fujisawa S., Ito A., Mitsuoka C., Berberich T., Tosa Y., et al. SPM1 encoding a vacuole-localized protease is required for infection-related autophagy of the rice blast fungus Magnaporthe oryzae. FEMS Microbiol Lett 2009, 300:115-121.
62. Liu T.B., Liu X.H., Lu J.P., Zhang L., Min H., Lin F.C. The cysteine protease MoAtg4 interacts with MoAtg8 and is required for differentiation and pathogenesis in Magnaporthe oryzae. Autophagy 2010, 6:74-85.
63. Veneault-Fourrey C., Barooah M., Egan M., Wakley G., Talbot N.J. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 2006, 312:580-583.
64. Bolwell G.P., Bindschedler L.V., Blee K.A., Butt V.S., Davies D.R., Gardner S.L., et al. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 2002, 53:1367-1376.
65. Bradley D., Kjellbom P., Lamb C. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 1992, 70:21-30.
66. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 1994, 79:583-593.
67. Sasaki K., Iwai T., Hiraga S., Kuroda K., Seo S., Mitsuhara I., et al. Ten rice peroxidases redundantly respond to multiple stresses including infection with rice blast fungus. Plant Cell Physiol 2004, 45:1442-1452.
68. Ndimba B.K., Chivasa S., Hamilton J.M., Simon W.J., Slabas A.R. Proteomic analysis of changes in the extracellular matrix of Arabidopsis cell suspension cultures induced by fungal elicitors. Proteomics 2003, 3:1047-1059.
69. Egan M.J., Wang Z.Y., Jones M.A., Smirnoff N., Talbot N.J. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci U S A 2007, 104:11772-11777.
70. Skamnioti P., Henderson C., Zhang Z., Robinson Z., Gurr S.J. A novel role for catalase B in the maintenance of fungal cell-wall integrity during host invasion in the rice blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 2007, 20:568-580.
71. van Loon L.C., Rep M., Pieterse C.M.J. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 2006, 44:135-162.
72. Vigers A.J., Viedmann S., Roberts W.K., Legrand M., Selitrennikoff C.P., Fritig B. Thaumatin-like pathogenesis-related proteins are antifungal. Plant Sci 1992, 83:155-161.
73. Hugot K., Riviere M.P., Moreilhon C., Dayem M.A., Cozzitorto J., Arbiol G., et al. Coordinated regulation of genes for secretion in tobacco at late developmental stages: association with resistance against oomycetes. Plant Physiol 2004, 134:858-870.
74. Kim S.T., Kim S.G., Kang Y.H., Wang Y., Kim J.Y., Yi N., et al. Proteomics analysis of rice lesion mimic mutant (spl1) reveals tightly localized probenazole-induced protein (PBZ1) in cells undergoing programmed cell death. J Proteome Res 2008, 7:1750-1760.