Application of proteomics to investigate stress-induced proteins for improvement in crop protection

Plant Cell Reports

Volumn 30, Issue 5, 2011, Pages 745-763

  Afroz, Amber ^a   Ali, Ghulam Muhammad ^a   Mir, Asif ^b   Komatsu, Setsuko ^c  

^a NATIONAL AGRICULTURAL RESEARCH CENTRE   (Pakistan)

^b Institute of Information Technology   (Pakistan)

^c NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

Author keywords

Bacteria; Pathogenesis related proteins; Proteomics; Salicylic acid; Stresses

Indexed keywords

ANTIINFECTIVE AGENT; CYCLOPENTANE DERIVATIVE; HEAT SHOCK PROTEIN; JASMONIC ACID; OXYLIPIN; PATHOGENESIS RELATED PROTEINS, PLANT; PATHOGENESIS-RELATED PROTEINS, PLANT; PBZ1 PROTEIN, ORYZA SATIVA; PHYTOHORMONE; SALICYLIC ACID; VEGETABLE PROTEIN;

BACTERIUM; CROP; DRUG EFFECT; FUNGUS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; METHODOLOGY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGICAL STRESS; PLANT; PLANT DISEASE; PLANT GENE; PLANT IMMUNITY; PLANT LEAF; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; VIRUS;

ANTI-INFECTIVE AGENTS; BACTERIA; CROPS, AGRICULTURAL; CYCLOPENTANES; FUNGI; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HEAT-SHOCK PROTEINS; HOST-PATHOGEN INTERACTIONS; OXYLIPINS; PLANT DISEASES; PLANT GROWTH REGULATORS; PLANT IMMUNITY; PLANT LEAVES; PLANT PROTEINS; PLANTS; PROTEOMICS; SALICYLIC ACID; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; VIRUSES;

BACTERIA (MICROORGANISMS);

EID: 79954582758     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-010-0982-x     Document Type: Review

References (142)

1. Abbink TE, Peart JR, Mos TN, Baulcombe DC, Bol JF, Linthorst HJ (2002) Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants. Virology 295: 307-319.
2. Abeles FB, Bosshart RP, Forrence L, Habig WH (1970) Preparation and purification of glucanase and chitinase from bean leaves. Plant Physiol 47: 129-134.
3. Afroz A, Khan MR, Ahsan N, Komatsu S (2009) Comparative proteomic analysis of bacterial wilt susceptible and resistant tomato cultivars. Peptides 30: 1600-1607.
4. Afroz A, Khan MR, Komatsu S (2010) Proteomic analysis of tomato cultivars treated with growth elicitor's jasmonic acid and salicylic acid. Protein Pept Lett 17: 836-846.
5. Akram A, Ongena M, Duby F, Dommes J, Thonart P (2008) Systemic resistance and lipoxygenase-related defence response induced in tomato by Pseudomonas putida strain BTP1. BMC Plant Biol 8: 1-12.
6. Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defence. Annu Rev Phytol 42: 385-414.
7. Avni A, Edelman M, Rachailovich I, Aviv D, Fluhr R (1989) A point mutation in the glutathione peroxidase activity from Arabidopsis thaliana: molecular cloning and functional characterization. Eur J Biochem 216: 579-858.
8. Bachmann D, Rezzonico E, Retelska D, Chetelat A, Schaerer S, Beffa R (1998) Improvement of potato resistance to Phytophthora infestans by overexpressing antifungal hydrolases. In: 5th international workshop on pathogenesis-related proteins. Signaling pathways and biological activities. March 29-April 2, Aussois, France. Abstracts, p 57.
9. Baier M, Dietz K-J (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol 119: 1407-1414.
10. Bernier F, Berna A (2001) Germins and germin-like proteins: plant do-all proteins. But what do they do exactly. Plant Physiol Biochem 39: 545-554.
11. Birch RG (1997) Plant transformation: problems and strategies for practical application. Annu Rev Plant Physiol Plant Mol Biol 48: 297-326.
12. Block A, Schmelz E, Donnel PJO, Jones JB, Klee HJ (2005) Systemic acquired tolerance to virulent bacterial pathogen in tomato. Plant Physiol 138: 1481-1490.
13. Bowles DJ (1990) Defense-related proteins in higher plants. Ann Rev Biochem 59: 873-907.
14. Brizard JP, Carapito C, Delalande F, van Dorsselaer A, Brugidou C (2006) Proteome analysis of plant-virus interactome: comprehensive data for virus multiplication inside their hosts. Mol Cell Proteom 5: 2279-2297.
15. Campo S, Carrascal M, Coca M, Abian J, San Segundo B (2004) The defence response of germinating maize embryos against fungal infection: a proteomics approach. Proteomics 4: 383-396.
16. Campos A, Gonçalo da Costa GD, Coelho AV, Fevereiro P (2009) Identification of bacterial protein markers and enolase as a plant response protein in the infection of Olea europaea subsp. europaea by Pseudomonas savastanoi pv. Savastanoi. Eur J Plant Pathol 125: 603-616.
17. Casado-Vela J, Selles S, Martinez RB (2006) Proteomic analysis of tobacco mosaic virus-infected tomato (Lycopersicon esculentum M.) fruits and detection of viral coat protein. Proteomics 6: 196-206.
18. Chang CCC, Slesak I, Jorda L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpinska B, Stanisław Karpinski S (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 150: 670-683.
19. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102(52): 19237-19242.
20. Chen Z-Y, Brown RL, Rajasekaran K, Damann KE, Cleveland TE (2006) Identification of a maize kernel pathogenesis-related protein and evidence for its involvement in resistance to Aspergillus flavus infection and aflatoxin production. Phytopathology 96: 87-95.
21. Chen F, Yuan Y, Li Q, He Z (2007) Proteomic analysis of rice plasma membrane reveals proteins involved in early defence response to bacterial blight. Proteomics 7: 1529-1539.
22. Chivasa S, John M, Hamilton JH, Pringle RS, Ndimba BK, Simon WJ, Lindsey K, Slabas AR (2006) Proteomic analysis of differentially expressed proteins in fungal elicitor-treated Arabidopsis cell cultures. J Exp Bot 57(7): 1553-1562.
23. Cho S, Shin S, Kim K, Kim Y, Eun M, Cho B (2004) Enhanced expression of a gene encoding a nucleoside diphosphate kinase 1 (OsNDPK1) in rice plants upon infection with bacterial pathogens. Mol Cells 18: 390-395.
24. Cho K, Agrawal GK, Shibato J, Jung Y-H, Kim Y-K, Nahm BH, Jwa N-S, Tamogami S, Han O, Kohda K, Iwahashi H, Rakwal R (2007) Survey of differentially expressed proteins and genes in jasmonic acid treated rice seedling shoot and root at the proteomics and transcriptomics levels. J Proteome Res 6: 3581-3603.
25. Christensen AB, Cho BH, Naesby M, Gregersen PL, Brandt J, Madriz-Ordenana K, Collinge DB, Thordal-Christensen H (2002) The molecular characterization of two barley proteins establishes the novel PR-17 family of pathogenesis-related proteins. Mol Plant Pathol 3: 135-144.
26. Coaker GL, Willard B, Kinter M, Stockinger EJ, Francis DM (2004) Proteomic analysis of resistance mediated by Rcm 2. 0 and Rcm 5. 1, two loci controlling resistance to bacterial canker of tomato. Mol Plant Microbe Interact 17: 1019-1028.
27. Colditz F, Nyamsuren O, Niehaus K, Eubel H, Braun H-P, Krajinski F (2004) Proteomic approach: identification of Medicago truncatula proteins induced in roots after infection with the pathogenic oomycete Aphanomyces euteiches. Plant Mol Biol 55: 109-120.
28. Curto M, Camafeita LE, Lopez JA, Maldonado AM, Rubiales D, Jorrin J (2006) A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi). Proteomics 6: 163-174.
29. Deepak SA, Shibato J, Ishii H, Ogawa Y, Yoshida Y, Iwahashi H, Masuo Y, Agrawal GK, Rakwal R (2008) Proteomics approach for investigating the disease resistance using cucumber as model plant. Am J Biochem Biotechnol 4: 231-238.
30. Delalande F, Carapito C, Brizard JP, Brugidou C, van Dorsselaer A (2005) Multigenic families and proteomics: extended protein characterization as a tool for paralog gene identification. Proteomics 5: 450-460.
31. Diaz-Vivancos P, Rubio M, Mesonero V, Periago PM, Barcelo AR, Martinez-Gomez P, Hernandez JA (2006) The apoplastic antioxidant system in Prunus: response to long-term plum pox virus infection. J Exp Bot 57: 3813-3824.
32. Doxey AC, Yaish MWF, Moffatt BA, Griffith M, McConkey BJ (2007) Functional divergence in the Arabidopsis β-1, 3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Mol Biol Evol 24: 1045-1055.
33. Dubery IA, Slater V (1997) Induced defence responses in cotton leaf disks by elicitors from Verticillium dahliae. Phytochemistry 44: 1429-1434.
34. Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5: 193-198.
35. Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13: 1025-1033.
36. Elvira MI, Galdeano MM, Gilardi P, Garcia-Luque I, Serra MT (2008) Proteomic analysis of pathogenesis-related proteins (PRs) induced by compatible and incompatible interactions of pepper mild mottle virus (PMMoV) in Capsicum chinense L3 plants. J Exp Bot 59: 1253-1265.
37. Floerl S, Druebert C, Majcherczyk A, Karlovsky P, Kues U, Polle A (2008) Defence reactions in the apoplastic proteome of oilseed rape (Brassica napus var. napus) attenuate Verticillium longisporum growth but not disease symptoms. BMC Plant Biol 8: 1-15.
38. Gorlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8: 629-643.
39. Gorovits R, Akad F, Beery H, Vidavsky F, Mahadav A, Czosnek H (2007) Expression of stress-response proteins upon whitefly-mediated inoculation of Tomato yellow leaf curl virus in susceptible and resistant tomato plants. Mol Plant Microbe Interact 20: 1376-1383.
40. Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17: 994-999.
41. Harish S, Kavino M, Kumar N, Samiyappan R (2009) Differential expression of pathogenesis-related proteins and defense enzymes in banana: interaction between endophytic bacteria, Banana bunchy top virus and Pentalonia nigronervosa. Biocontrol Sci Technol 19: 843-857.
42. Hase S, Takenaka S, Nakaho K, Arie T, Seo S, Ohashi Y, Takahashi H (2008) Involvement of jasmonic acid signaling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol 57: 870-876.
43. Hooft van Huijsduijnen RAM, Alblas SWDE, Rijk RH, Bol JF (1986) Induction by salicylic acid of pathogenesis-related proteins and resistance to Alfalfa Mosaic Virus infection in various plant species. J Gen Virol 67: 2135-2143.
44. Houterman PM, Speijer D, Dekker HL, Koster CGD, Cornelissen BJC, Rep M (2007) The mixed xylem sap proteome of Fusarium oxysporium infected tomato plants. Mol Plant Pathol 8: 215-221.
45. Husaini AM, Zainul Abdin M (2008) Overexpression of tobacco osmotin gene leads to salt stress tolerance in strawberry (Fragaria × ananassa Duch.) plants. Ind J Plant Biotech 7: 465-471.
46. Ishikawa T (1992) The ATP-dependent glutathione S-conjugate export pump. Trends Biochem Sci 17: 463-468.
47. Issaq HJ, Chan KC, Janini GM, Conrads TP, Veenstra TD (2005) Multidimensional separation of peptides for effective proteomic analysis. J Chromatogr B Analyt Technol Biomed Life Sci 817: 35-47.
48. Jain SK, Lim G (2001) Pyridoxine and pyridoxamine inhibit superoxide radicals and prevent lipid peroxidation, protein glycosylation and (NaCCKC)-ATPase activity reduction in high glucose-treated human erythrocytes. Free Radic Biol Med 30: 232-237.
49. Jiang Q, Chen H, Pan X, Pan Q, Shi Y, Li X, Zhang G, Wang Y, Xie S, Shen S (2008) Proteomic analysis of wheat (Triticum aestivum L.) hybrid necrosis. Plant Sci 175: 394-401.
50. Jin B, Jiang F, Yu M, Chen N, Ding Z (2009) Agrobacterium tumefaciens mediated chitinase and beta-1, 3-glucanase gene transformation for Pinellia ternate. Zhongguo Zhong Yao Za Zhi 34(14): 1765-1767.
51. Jones AME, Thomas V, Truman B, Lilley K, Mansfield J, Grant M (2004) Specific changes in the Arabidopsis proteome in response to bacterial challenge: differentiating basal and R-gene mediated resistance. Phytochemistry 65: 1805-1816.
52. Jones AME, Thomas V, Bennett MH, Mansfield J, Grant M (2006a) Modifications to the Arabidopsis defence proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol 142: 1603-1620.
53. Jones AME, Bennett MH, Mansfield JW, Grant M (2006b) Analysis of the defence phosphoproteome of Arabidopsis thaliana using differential mass tagging. Proteomics 6: 4155-4165.
54. Kandasamy S, Loganathan K, Muthuraj R, Duraisamy S, Seetharaman S, Thiruvengadam R, Ponnusamy B, Ramasamy S (2009) Understanding the molecular basis of plant growth promotional effect of Pseudomonas fluorescens on rice through protein profiling. Proteome Sci 7(47): 1-7.
55. Kim JK, Jang IC, Wu R, Zuo WN, Boston RS, Lee YH, Ahn IP, Nahm BH (2003a) Co-expression of a modified maize ribosome-inactivating protein and a rice basic chitinase gene in transgenic rice plants confers enhanced resistance to sheath blight. Transgenic Res 12: 475-484.
56. Kim ST, Cho KS, Yu S, Kim SG, Hong JC, Han CD, Bae DW, Nam MH, Kang KY (2003b) Proteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells. Proteomics 3: 2368-2378.
57. Kim ST, Kim SG, Hwang DH, Kang SY, Kim HJ, Lee BH, Lee JJ, Kang KY (2004) Proteomic analysis of pathogen-responsive proteins from rice leaves induced by rice blast fungus, Magnaporthe grisea. Proteomics 4: 3569-3578.
58. Kim KH, Alam I, Lee K-W, Sharmin SA, Kwak S-S, Lee SY, Lee B-H (2009) Enhanced tolerance of transgenic tall fescue plants overexpressing 2-Cys peroxiredoxin against methyl viologen and heat stresses. Biotech Lett 32(4): 571-576.
59. Komatsu S, Konishi H, Shen S, Yang G (2003) Rice proteomics: a step toward functional analysis of the rice genome. Mol Cell Proteom 2: 2-10.
60. Kumar SM, Kumar BK, Sharma KK, Devi P (2004) Genetic transformation of pigeonpea with rice chitinase gene. Plant Breed 123: 485-489.
61. Kumari GJ, Reddy AM, Naik ST, Kumar SG, Prasanthi J, Sriranganayakulu G, Reddy PC, Sudhakar C (2006) Jasmonic acid induced changes in protein pattern, antioxidative enzyme activities and peroxidase isozymes in peanut seedlings. Biol Plantarum 50(2): 219-226.
62. Kurkcuoglu S, Piotrowski M, Gau AE (2004) Up-regulation of pathogenesis related proteins in the apoplast of Malus domestica after application of a non-pathogenic bacterium. J Biosci 59: 843-848.
63. Lagrimini LM, Bradford S, Steven Rothstein S (1990) Peroxidase-induced wilting in transgenic tobacco plants. Plant Cell 2: 7-18.
64. Lagrimini LM (1991) Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96: 577-583.
65. Lagrimini LM, Joly RJ, Dunlap JR, Liu T-TY (1997) The consequence of peroxidase over expression in transgenic plants on root growth and development. Plant Mol Biol 33: 887-895.
66. Lawrence CB, Joosten MHAJ, Tuzun S (1996) Differential induction of pathogenesis-related proteins in tomato by Alternaria solani and the association of a basic chitinase isozyme with resistance. Physiol Mol Plant Pathol 48(6): 361-377.
67. Lee J, Bricker TM, Lefevre M, Pinson SRM, Oard JH (2006a) Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia Solani. Mol Plant Pathol 7(5): 405-416.
68. Lee BJ, Kwon SJ, Kim SK, Kim KJ, Park CJ, Kim YJ, Park OK, Paek KH (2006b) Functional study of hot pepper 26S proteasome subunit RPN7 induced by tobacco mosaic virus from nuclear proteome analysis. Biochem Biophys Res Commun 351: 405-411.
69. Lifang W, Hong L, Huiyun F, Lijun W, Zengliang Y (2001) Introduction of rice chitinase gene into wheat via low energy Ar + beam implantation. Chin Sci Bull 46(4): 318-322.
70. Lin Y-Z, Chen H-Y, Kao R, Chang S-P, Chang S-J, Lai E-M (2008) Proteomic analysis of rice defense response induced by probenazole. Phytochemistry 69(3): 715-728.
71. Linthorst HJM, Melchers LS, Mayer A, van Roekel JSC, Cornelissen BJC, Bol JF (1990) Analysis of gene families encoding acidic and basic-1, 3 glucanases of tobacco. Proc Natl Acad Sci USA 87: 8756-8760.
72. Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10: 371-382.
73. MacBeath G (2002) Protein microarrays and proteomics. Nat Genet 32(Suppl): 526-532.
74. Mahmood T, Jan A, Kakishima M, Komatsu S (2006) Proteomic analysis of bacterial-blight defence responsive proteins in rice leaf blades. Proteomics 6: 6053-6065.
75. Mahmood T, Kakishima M, Komatsu S (2009) Proteome analysis of probenazol-effect in rice-bacterial blight infection. Protein Pept Lett 16: 1041-1052.
76. Marcus BS, Daniel M, Flavia VW, Carlos Eduardo S, Rafael RC, Fernanda F, Itaraju Junior B, Eduardo G, Helvecio Filho DC, Marcos Antonio M, Sergio M, Jose Camillo N (2003) Proteome analysis of the plant pathogen Xylella fastidiosa reveals major cellular and extracellular proteins and a peculiar codon bias distribution. Proteomics 3: 224-237.
77. Marouga R, David S, Hawkins E (2005) The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 382: 669-678.
78. Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 127-158.
79. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100: 1444-1449.
80. Mauch F, Staehelin LA (1989) Functional implications of the subcellular localization of ethylene-induced chitinase and beta-1, 3-glucanase in bean leaves. Plant Cell 1: 447-457.
81. McFadden HG, Chapple R, de Feyter R, Dennis E (2001) Expression of pathogenesis-related genes in cotton stems in response to infection by Verticillium dahliae. Physiol Mol Plant Pathol 58: 119-131.
82. Melchers LS, Apotheker-de Groot M, van der Knaap JA, Ponstein AS, Sela-Buurlage MB, Bol JF, Cornelissen BJC, van den Elzen PJM, Linthorst HJM (1994) A new class of tobacco chitinases homologous to bacterial exo-chitinases displays antifungal activity. Plant J 5: 469-480.
83. Melchers LS, Lageweg W, Stuiver MH (1998) The utility of PR genes to develop disease resistance in transgenic crops. In: 5th international workshop on pathogenesis- related proteins. Signalling pathways and biological activities. March 29-April 2, 1998, Aussois, France. Abstracts, p 46.
84. Metraux J-P, Streit L, Th Staub (1988) A pathogenesis-related protein in cucumber is a chitinase. Physiol Mol Plant Pathol 33: 1-9.
85. Metraux JP, Nawrath C, Genoud T (2002) Systemic acquired resistance. Euphytica 124: 237-243.
86. Miao L, Shou S, Zhu Z, Jiang F, Zai W, Yang Y (2008) Isolation of a novel tomato Caffeoyl CoA 3-O-methyltransferase gene following infection with bacterium Ralstonia solanacearum. J Phytopathol 156: 588-596.
87. Mittler R, Herr EH, Orvar BL, Camp WV, Willekens H, Inze D, Brian E, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc Natl Acad Sci USA 96(24): 14165-14170.
88. Moons A, Prinsen E, Bauw G, Montaguasi MV (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9: 2243-2259.
89. Moschou PN, Delis LD, Paschalidis KA, Roubelakis-Angelakis KA (2008) Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiol Plant 133(2): 140-156.
90. Na JK, Allen RD, You YS, Song YS, Song YN, Lim HT (1998) Genetic transformation of ascorbate peroxidase gene into potato plant, Solanum tubersoum. PAA meeting in Fargo, USA.
91. Niderman T, Genetet I, Bruyere T, Gees R, Stintzi A, Legrand M, Fritig B, Mosinger E (1995) Pathogenesis-related PR-1 proteins are antifungal. Isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol 108: 17-27.
92. Okushima Y, Koizumi N, Kusano T, Sano H (2000) Secreted proteins of tobacco cultured BY2 cells: identification of a new member of pathogenesis-related proteins. Plant Mol Biol 42: 479-488.
93. Park C-J, Kim K-J, Shin R, Park JM, Shin Y-C, Peak K-H (2004a) Pathogenesis related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J 37: 186-198.
94. Park C-J, An J-M, Shin Y-C, Kim K-J, Lee B-J, Paek K-H (2004b) Molecular characterization of pepper germin-like protein as the novel PR-16 family of pathogenesis related proteins isolated during the resistance response to viral and bacterial infection. Planta 219: 797-806.
95. Park Y-S, Jeon MH, Lee S-H, Moon JS, Cha J-S, Kim HY, Cho T-J (2005) Activation of defense responses in chinese cabbage by a non host pathogen, Pseudomonas syringae pv. tomato. J Biochem Mol Biol 38: 748-754.
96. Perez-Bueno ML, Rahoutei J, Sajnani C, Garcia-Luque I, Baron M (2004) Proteomic analysis of the oxygen evolving complex of photosystem II under biotic stress: studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4: 418-425.
97. Pieterse CMJ, van Loon LC (1999) Salicylic acid independent plant defense pathways. Trends Plant Sci 4: 52-58.
98. Pires Leitao TM, Romero J, Duran-Vila N (1993) Detection of pathogenesis related proteins associated with viroid infection in citrus. Citrus Viroids. Twelfth ZOCV conference, pp 196-201.
99. Popowich EA, Firsov AP, Mitiouchkina TY, Filipenya VL, Dolgov SV, Reshetnikov VN (2007) Agrobacterium-mediated transformation of Hyacinthus orientalis with thaumatin II gene to control fungal diseases. Plant Cell Tissue Organ Cult 90(3): 237-244.
100. Pos V, Halasz K, Mesterhazi A, Csosz L, Manninger K, Hunyadi-Gulyas E, Medzihradszky K, Juhasz T, Lukacs N (2005) Proteomic investigation of wheat intercellular washing fluid. Proceedings of the 8th Hungarian congress on plant physiology and the 6th Hungarian conference on photosynthesis. Acta Biol Szegediensis 49: 31-32.
101. Quilis J, Penas G, Joaquima Messeguer J, Brugidou C, Segundo BS (2008) The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol Plant Microbe Interact 21(9): 1215-1231.
102. Radhajeyalakshmi R, Velazhahan R, Samiyappan R, Doraiswamy S (2009) Systemic induction of pathogenesis related proteins (PRs) in Alternaria solani elicitor sensitized tomato cells as resistance response. Sci Res Essay 4: 685-689.
103. Rahoutei J, Garcia-Luque I, Baron M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol Plant 110: 286-292.
104. Rakwal R, Agrawal GK, Yonekura M (1999) Separation of proteins from stressed rice (Oryza sativa L.) leaf tissues by two-dimensional polyacrylamide gel electrophoresis: Induction of pathogenesis related and cellular protectant proteins by jasmonic acid, UV irradiation and copper chloride. Electrophoresis 20(17): 3472-3478.
105. Rakwal R, Komatsu S (2000) Role of jasmonate in the rice self defense mechanism using proteome analysis. Electrophoresis 21(12): 2492-2500.
106. Rakwal R, Komatsu S (2001) Jasmonic acid-induced necrosis and drastic decreases in ribulose-1, 5-bisphosphate carboxylase/oxygenase in rice seedlings under light involves reactive oxygen species. J Plant Physiol 158(6): 679-688.
107. Ramamoorthy V, Raguchander T, Samiyappan R (2002) Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. Lycopersici. Plant Soil 239: 55-68.
108. Rep M, Dekker HL, Vossen JH, de Boer AD, Houterman PM, Speijer D, Back JW, de Koster CG, Cornelissen BJC (2002) Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus infected tomato. Plant Physiol 130: 904-917.
109. Rickauer M, Brodschelm W, Bottin A, Veronesi C, Grimal H, Esquerre-Tugaye MT (1997) The jasmonate pathway is involved differentially in the regulation of different defense responses in tobacco cells. Planta 202: 155-162.
110. Rodrigo I, Vera P, Frank R, Conejero V (1991) Identification of the viroid-induced tomato pathogenesis-related (PR) protein P23 as the thaumatin-like tomato protein NP24 associated with osmotic stress. Plant Mol Biol 16: 931-934.
111. Rose JKC, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39: 715-733.
112. Rosen R, Sacher A, Shechter N, Becher D, Buttner K, Biran D, Hecker M, Ron EZ (2004) Two-dimensional reference map of Agrobacterium tumefaciens proteins. Proteomics 4: 1061-1073.
113. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteom 3: 1154-1169.
114. Ryang S-H, Chung S-Y, Lee S-H, Cha J-S, Kim HY, Cho T-J (2002) Isolation of pathogen-induced Chinese cabbage genes by subtractive hybridization employing selective adaptor ligation. Biochem Biophys Res Comm 299: 352-359.
115. Sadat Noori SA, Sokhansanj A (2008) Wheat plants containing an osmotin gene show enhanced ability to produce roots at high NaCl concentration. Russ J Plant Physiol 55(2): 256-258.
116. Salekdeh GH, Komatsu S (2007) Crop proteomics: aim at sustainable agriculture. Proteomics 7: 2976-2996.
117. Sarowar S, Kim YJ, Kim EN, Kim KD, Hwang BK, Islam R, Shin JS (2005) Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep 24: 216-224.
118. Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44(4): 653-668.
119. Schestibratov KA, Dolgov SV (2005) Transgenic strawberry plants expressing a thaumatin II gene demonstrate enhanced resistance to Botrytis cinerea. Sci Horticult 106: 177-189.
120. Selitrennikoff CP (2001) Antifungal proteins. Appl Env Microbiol 67: 2883-2894.
121. Shimono M, Yazaki J, Nakamura K, Kishimoto N, Kikuchi S, Iwano M, Yamamoto K, Sakata K, Sasaki T, Nishiguchi M (2003) cDNA microarray analysis of gene expression in rice plants treated with probenazole, a chemical inducer of disease resistance. J Gen Plant Pathol 69: 76-82.
122. Shin S, Mackintosh CA, Lewis J, Heinen SJ, Radmer L, Dill-Macky R, Baldridge GD, Zeyen RJ, Muehlbauer GJ (2008) Transgenic wheat expressing a barley class II chitinase gene has enhanced resistance against Fusarium graminearum. J Exp Bot 59(9): 2371-2378.
123. Sreeramanan S, Maziah M, Xavier R (2009) A protocol for Agrobacterium-mediated transformation of banana with a rice chitinase gene. Emir J Food Agric 21(2): 18-33.
124. Subramanian B, Bansal VK, Kav NN (2005) Proteome-level investigation of Brassica carinata derived resistance to Leptosphaeria maculans. J Agric Food Chem 53: 313-324.
125. Takahashi W, Fujimori M, Miura Y, Komatsu T, Nishizawa Y, Hibi T, Takamizo T (2005) Increased resistance to crown rust disease in transgenic Italian ryegrass (Lolium multiflorum Lam.) expressing the rice chitinase gene. Plant Cell Rep 23: 811-818.
126. Todd MJ, Lorimer GH, Thirumalai D (1996) Chaperonin-facilitated protein folding: Optimization of rate and yield by an iterative annealing mechanism. Proc Natl Acad Sci USA 93: 4030-4035.
127. Tohidfar M, Mohammadi M, Ghareyazie M, Ghareyazie B (2006) Agrobacterium-mediated transformation of cotton (Gossypium hirsutum) using a heterologous bean chitinase gene. Plant Cell Tissue Organ Cult 83: 83-96.
128. Toorchi M, Yukawa K, Nouri M-Z, Komatsu S (2009) Proteomics approach for identifying osmotic-stress-related proteins in soybean roots. Peptides 30: 2108-2117.
129. Tsunezuka H, Fujiwara M, Kawasaki T, Shimamoto K (2005) Proteome analysis of programmed cell death and defense signaling using the rice lesion mimic mutant cdr2. Mol Plant Microbe Interact 18(1): 52-59.
130. Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18: 2071-2077.
131. van Loon LC (1982) Regulation of changes in proteins and enzymes associated with active defense against virus infection. In: Wood RKS (ed) Active defense mechanisms in plants. Plenum Press, New York, pp 247-273.
132. van Loon LC (1999) Occurrence and properties of plant pathogenesis-related proteins. In: Datta SK, Mathukrishnan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, pp 1-19.
133. van Loon LC, van Kammen A (1970) Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. "Smsun" and "Samsun NN" II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 40: 199-206.
134. Vitamvas P, Kosova K, Prasil IT (2007) Proteome analysis in plant stress research. Czech J Genet Plant Breed 43: 1-6.
135. Washburn MP, Wolters D, Yates JR (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotech 19: 242-247.
136. Wu CT, Bradford KJ (2003) Class I chitinase and 1, 3-glucanase are differentially regulated by wounding, methyl jasmonate, ethylene, and gibberellin in tomato seeds and leaves. Plant Physiol 133: 263-273.
137. Xu Y, Chang PFL, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6: 1077-1085.
138. Yu T, Li YS, Chen XF, Hu J, Chang X, Zhu YG (2003) Transgenic tobacco plants overexpressing cotton glutathione S-transferase (GST) show enhanced resistance to methyl viologen. J Plant Physiol 160(11): 1305-1311.
139. Zhou XJ, Lu S, Xu YH, Wang JW, Chen XY (2002) A cotton cDNA (GaPR-10) encoding a pathogenesis-related 10 protein with in vitro ribonuclease activity. Plant Sci 162: 629-636.
140. Zhou W, Eudes F, Laroche A (2006) Identification of differentially regulated proteins in response to a compatible interaction between the pathogen Fusarium graminearum and its host, Triticum aestivum. Proteomics 6: 4599-4609.
141. Zieske LR (2006) A perspective on the use of iTRAQ reagent technology for protein complex and profiling studies. J Exp Bot 57: 1501-1508.
142. Zou J, Rodriguez-Zas S, Aldea M, Li M, Zhu J, Gonzalez DO, Vodkin LO, DeLucia E, Clough SJ (2005) Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis. Mol Plant Microbe Interact 18: 1161-1174.