Proteomic Studies Revealing Enigma of Plant–Pathogen Interaction

  • Anjana Rustagi
  • Garvita Singh
  • Shachi Agrawal
  • Prem Kumar Gupta
Chapter

Abstract

Pathogen attack is an intricate stimulus that induces stepwise defence response, namely, pathogen recognition, signal transduction and accomplishment of resistance/defense. These steps employ an array of proteins, interacting among themselves to sense the pathogen and produce antimicrobials antagonistic to pathogen growth. In order to gain insights in molecular mechanism of plant–pathogen interaction at the biochemical and cellular level, deciphering the proteins that are involved in this cellular medley is a prerequisite. Proteomics, one of the important subjects of “OMICS” generation, has played a principal role in the identification of these proteins. Proteomics aims at identification and quantification of the proteins mediating a specific cellular process. While the current proteomic studies give valid information about these processes, they also emphasize upon the significance of post-translational modifications. The information on sequence and post-translational modifications of proteins is then used to further decipher the biological processes using bioinformatics, genomics, cell biology, biochemistry and other areas of life sciences. We present a brief overview of the proteomic studies related to host–virus, host–bacteria and host–fungus interaction. We also provide the current stage of information on the techniques applied in proteomics and also the future challenges in this area of biological science.

Keywords

Proteomics Plant–pathogen interaction Two-dimensional polyacrylamide gel electrophoresis (2D-PAGE) Fluorescent two-dimensional differencial gel electrophoresis (2D-DIGE) ICAT (Isotope-coded affinity tags) ITRAQ (Isobaric tagged for relative and absolute quantitation) MudPIT (Multidimensional protein identification technology) Mass spectrometry (MS) Protein microarray 

Notes

Acknowledgement

The authors would like to acknowledge the kind help of Dr. Shalu Jain, Plant Pathology Division, North Dakota State University, Fargo, USA, for critical comments and suggestions.

References

  1. Abdallah C, Dumas-Gaudot E, Renaut J et al (2012) Gel-based and gel-free quantitative proteomics approaches at a glance. Int J Plant Genom 2012:Article ID 494572., 17 pages. https://doi.org/10.1155/2012/ 494572 Google Scholar
  2. Agarwal K, Choe LH, Lee KH (2006) Shotgun proteomics using the iTRAQ isobaric tags. Brief Funct Genom Proteomics 5(2):112–120CrossRefGoogle Scholar
  3. Agrawal GK, Jwa NS, Lebrun MH et al (2010) Plant secretome: unlocking secrets of the secreted proteins. Proteomics 10:799–827PubMedCrossRefGoogle Scholar
  4. Anderson DC, Campbell EL, Meeks JC (2006) A soluble 3D LC/MS/MS proteome of the filamentous cyanobacterium Nostoc punctiforme. J Proteome Res 5:3096–3104PubMedCrossRefGoogle Scholar
  5. Andrade AE, Silva LP, Pereira JL et al (2008) In vivo proteome analysis of Xanthomonas campestris pv. campestris in the interaction with the host plant Brassica oleracea. FEMS Microbiol Lett 281:167–174PubMedCrossRefGoogle Scholar
  6. Anguraj-Vadivel AK (2015) Gel-based proteomics in plants: time to move on from the tradition. Front Plant Sci 6:369PubMedPubMedCentralCrossRefGoogle Scholar
  7. Asai S, Shirasu K (2015) Plant cells under siege: plant immune system versus pathogen effectors. Curr Opin Plant Biol 28:1–8PubMedCrossRefGoogle Scholar
  8. Babich R, Katam R (2016) Leaf proteome profiling and their interactions to determine disease resistance in Grape. Book of Abstract ‘Plant and Animal genome conference XXIV’ January 08–13, 2016 San Diego, CAGoogle Scholar
  9. Bertone P, Snyder M (2005) Advances in functional protein microarray technology. FEBS J 272:5400–5411PubMedCrossRefGoogle Scholar
  10. Bohmer M, Colby T, Bohmer C et al (2007) Proteomic analysis of dimorphic transition in the phytopathogenic fungus Ustilago maydis. Proteomics 7:675–685PubMedCrossRefGoogle Scholar
  11. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406PubMedCrossRefGoogle Scholar
  12. Bosch G, Skovran E, Xia Q et al (2008) Comprehensive proteomics of methylobacterium extorquens AM1 metabolism under single carbon and non methylotrophic conditions. Proteomics 8:3494–3505PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brizard JP, Carapito C, Delalande F et al (2006) Proteome analysis of plant–virus interactome: comprehensive data for virus multiplication inside their hosts. Mol Cell Proteomics 5:2279–2297PubMedCrossRefGoogle Scholar
  14. Buttner D, Bonas U (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 34:107–133PubMedCrossRefGoogle Scholar
  15. Campo S, Carrascal M, Coca M et al (2004) The defence response of germinating maize embryos against fungal infection: a proteomics approach. Proteomics 4(2):383–396PubMedCrossRefGoogle Scholar
  16. Cantin GT, Venable JD, Cociorva D et al (2006) Quantitative phosphoproteomic analysis of the tumor necrosis factor pathway. J Proteome Res 5(1):127–134PubMedPubMedCentralCrossRefGoogle Scholar
  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(Suppl. 1):S196–S206PubMedCrossRefGoogle Scholar
  18. Chen F, Yuan Y, Li Q et al (2007) Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight. Proteomics 7:1529–1539PubMedCrossRefGoogle Scholar
  19. Chivasa S, Hamilton JM, Pringle RS et al (2006) Proteomic analysis of differentially expressed proteins in fungal elicitor-treated Arabidopsis cell cultures. J Expt Bot 57(7):1553–1562CrossRefGoogle Scholar
  20. Chung WJ, Shu HY, Lu C et al (2007) Qualitative and comparative proteomic analysis of Xanthomonas campestris pv. Campestris17. Proteomics 7:2047–2058PubMedCrossRefGoogle Scholar
  21. Coaker GL, Willard B, Kinter M et al (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 17:1019–1028PubMedCrossRefGoogle Scholar
  22. Cooper B, Clarke JD, Budworth P et al (2003) A network of rice genes associated with stress response and seed development. Proc Natl Acad Sci U S A 100:4945–4950PubMedPubMedCentralCrossRefGoogle Scholar
  23. Corbett M, Virtue S, Bell K et al (2005) Identification of a new quorum-sensing controlled virulence factor in Erwinia carotovora subsp. Atroseptica secreted via the type II targeting pathway. Mol Plant-Microbe Interact 18:334–342PubMedCrossRefGoogle Scholar
  24. De-Blasio SL, Johnson R, Sweeney MM et al (2015) The potato leafroll virus structural proteins manipulate overlapping, yet distinct protein interaction networks during infection. Proteomics 15(12):2098–2112CrossRefGoogle Scholar
  25. Delalande F, Carapito C, Brizard JP et al (2005) Multigenic families and proteomics: extended protein characterization as a tool for paralog gene identification. Proteomics 5:450–460PubMedCrossRefGoogle Scholar
  26. Delaunois B, Jeandet P, Clément C et al (2014) Uncovering plant-pathogen crosstalk through apoplastic proteomic studies. Front Plant Sci 5(249):1–18Google Scholar
  27. Demirci YE, Inan C, Gunel A et al (2016) Proteome profiling of the compatible interaction between wheat and stripe rust. Eur J Plant Pathol 145(4):941–962CrossRefGoogle Scholar
  28. Devos S, Laukens K, Deckers P et al (2006) A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis. Mol Plant-Microbe Interact 19:1431–1443PubMedCrossRefGoogle Scholar
  29. Diaz-Vivancos P, Rubio M, Mesonero V et al (2006) The apoplastic antioxidant system in Prunus: response to long-term plum pox virus infection. J Exp Bot 57:3813–3824PubMedCrossRefGoogle Scholar
  30. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant– pathogen interactions. Nat Rev Genet 11(8):539–548PubMedCrossRefGoogle Scholar
  31. Doehlemann G, Hemetsberger C (2013) Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol 198:1001–1016PubMedCrossRefGoogle Scholar
  32. Duley H, Grover A (2001) Current initiatives in proteomics research: the plant perspective. Curr Sci 80(2):262–269Google Scholar
  33. Ekramoddoullah AKM, Hunt RS (1993) Changes in protein profile of susceptible and resistant sugar-pine foliage infected with the Whitepine blister rust fungus Cronartium ribicola. Can J Plant Pathol 15(4):259–264CrossRefGoogle Scholar
  34. Ellis JG, Dodds PN, Lawrence GJ (2007) The role of secreted proteins in diseases of plants caused by rust, powdery mildew and smut fungi. Curr Opin Microbiol 10:326–331PubMedCrossRefGoogle Scholar
  35. Feng X, Liu BF, Li J et al (2015) Advances in coupling microfluidic chips to mass spectrometry. Mass Spectrom Rev 34(5):535–557PubMedCrossRefGoogle Scholar
  36. Fenn JB, Mann M, Meng CK et al (1989) Electrospray ionization for mass spectrometry of large biomolecules. Science 246:64–71PubMedCrossRefGoogle Scholar
  37. Fey SJ, Larsen PM (2001) 2D or not 2D two-dimensional gel electrophoresis. Curr Opin Chem Biol 5:26–33PubMedCrossRefGoogle Scholar
  38. Flajsman M, Mandelc S, Radisek S et al (2016) Identification of novel virulence-associated proteins secreted to xylem by Verticillium nonalfalfae during colonization of hop plants. Mol Plant Microbe Interact 29(5):362–373PubMedCrossRefGoogle Scholar
  39. Gao W (2014) Analysis of protein changes using two-dimensional difference gel electrophoresis. Mol Toxicol Protocol 1105:17–30CrossRefGoogle Scholar
  40. Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011PubMedCrossRefGoogle Scholar
  41. Gonzalez-Fernandez R, Jorrin-Novo JV (2010) Proteomics of fungal plant pathogens: the case of Botrytis cinerea. In: Méndez-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology. FORMATEX, Badajoz, pp 205–217Google Scholar
  42. Gorg A, Weiss W, Dunn M (2004) Current two-dimensional electrophoresis technology for proteomics. Proteomics 4(12):3665–3685PubMedCrossRefGoogle Scholar
  43. Gourion B, Rossignol M, Vorholt JA (2006) A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. Proc Natl Acad Sci U S A 103:13186–13191PubMedPubMedCentralCrossRefGoogle Scholar
  44. Grenville-Briggs LJ, Avrova AO, Bruce CR et al (2005) Elevated amino acid biosynthesis in Phytophthora infestans during appressorium formation and potato infection. Fungal Genet Biol 42:244–256PubMedCrossRefGoogle Scholar
  45. Guerreiro N, Redmond JW, Rolfe BG et al (1997) New Rhizobium leguminorum flavonoid induced proteins revealed by proteome analysis of differentially displayed proteins. Mol Plant-Microbe Interact 10:506–516PubMedCrossRefGoogle Scholar
  46. Gygi SP, Rist B, Gerber SA et al (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17(10):994–999PubMedCrossRefGoogle Scholar
  47. Hall DA, Zhu H, Zhu X et al (2004) Regulation of gene expression by a metabolic enzyme. Science 306:482–484PubMedCrossRefGoogle Scholar
  48. Hammond-Kosack KE, Jones JDG (2000) Responses to plant pathogens. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiology, Rockville, pp 1102–1156Google Scholar
  49. Han X, Aslanian A, Yates JR (2008) Mass spectrometry for proteomics. Curr Opin C Biol 12(5):483–490CrossRefGoogle Scholar
  50. Hernandez LG, Lu B, Da Cruz GC et al (2012) Worker honeybee brain proteome. J Proteome Res 11:1485–1493PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hogenhout SA, Van der Hoorn RA, Terauchi R et al (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant-Microbe Interact 22:115–122PubMedCrossRefGoogle Scholar
  52. Hoving S, Voshol H, Oostrum J (2000) Towards high performance two-dimensional gel electrophoresis using ultrazoom gels. Electrophoresis 21:2617–2621PubMedCrossRefGoogle Scholar
  53. Issaq HJ, Chan KC, Janini GM et al (2005) Multidimensional separation of peptides for effective proteomic analysis. J Chromatogr B 817(1):35–47CrossRefGoogle Scholar
  54. Jacobs JM, Babujee L, Meng F et al (2012) The in planta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato. MBio 3:112–114CrossRefGoogle Scholar
  55. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  56. Jones AME, Thomas V, Truman B et al (2004) Specific changes in the Arabidopsis proteome in response to bacterial challenge: differentiating basal and R-gene mediated resistance. Phytochemistry 65:1805–1816PubMedCrossRefGoogle Scholar
  57. Jones AME, Thomas V, Bennett MH et al (2006) Modifications to the Arabidopsis defence proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol 142:1603–1620PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kandasamy S, Loganathan K, Muthuraj R et al (2009) Understanding the molecular basis of plant growth promotional effect of Pseudomonas fluorescens on rice through protein profiling. Proteome Sci 7:47PubMedPubMedCentralCrossRefGoogle Scholar
  59. Karas M, Hillenkamp F (1988) Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Anal Chem 60:2299–2301PubMedCrossRefGoogle Scholar
  60. Karunakaran R, Ramachandran VK, Seaman JC et al (2009) Transcriptomic analysis of Rhizobium leguminosarum biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol 191:4002–4014PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kazemi-Pour N, Condemine G, Hugouvieux-Cotte-Pattat N (2004) The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 4:3177–3186PubMedCrossRefGoogle Scholar
  62. Kundu S, Chakraborty D, Pal A (2011) Proteomic analysis of salicylic acid induced resistance to Mungbean yellow mosaic India virus in Vigna mungo. J Proteome 74:337–349CrossRefGoogle Scholar
  63. Kwon YS, Lee DY, Rakwal R et al (2016) Proteomic analyses of the interaction between the plant-growth promoting Rhizobacterium paenibacillus polymyxa E681 and Arabidopsis thaliana. Proteomics 1:122–135CrossRefGoogle Scholar
  64. Larrainzar E, Wienkoop S, Weckwerth W et al (2007) Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiol 144:1495–1507PubMedPubMedCentralCrossRefGoogle Scholar
  65. Larsen MKG, Jorgensen MM, Bennike TB et al (2016) Time-course investigation of Phytophthora infestans infection of potato leaf from three cultivars by quantitative proteomics. Elsevier Data Brief 6:238–248CrossRefGoogle Scholar
  66. Lee BJ, Kwon SJ, Kim SK et al (2006) Functional study of hot pepper 26S proteasome subunit RPN7 induced by tobacco mosaic virus from nuclear proteome analysis. Biochem Biophys Res Commun 351:405–411PubMedCrossRefGoogle Scholar
  67. Liang Y, Srivastava S, Rahman MH et al (2008) Proteome changes in leaves of Brassica napus L. as a result of Sclerotinia sclerotiorum challenge. J Agric Food Chem 56(60):1963–1976PubMedCrossRefGoogle Scholar
  68. Lo Presti L, Lanver D, Schweizer G et al (2015) Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66:513–545PubMedCrossRefGoogle Scholar
  69. Lodha TD, Basak J (2012) Plant-pathogen interaction: what microarray tells about it? Mol Biotechnol 50(1):87–97PubMedCrossRefGoogle Scholar
  70. Lodha TD, Hembram P, Tep N et al (2013) Proteomics: a successful approach to understand the molecular mechanism of plant-pathogen interaction. Am J Plant Sci 4:1212–1226CrossRefGoogle Scholar
  71. Lund TC, Anderson LB, McCullar V (2007) iTRAQ is a useful method to screen for membrane-bound proteins differentially expressed in human natural killer cell types. J Proteome Res 6:644–653PubMedCrossRefGoogle Scholar
  72. Ma B (2015) Novor: real-time peptide de novo sequencing software. J Am Soc Mass Spectrom 26:1885–1894PubMedPubMedCentralCrossRefGoogle Scholar
  73. Mahmood T, Jan A, Kakishima M et al (2006) Proteomic analysis of bacterial-blight defence responsive proteins in rice leaf blades. Proteomics 6:6053–6065PubMedCrossRefGoogle Scholar
  74. Mandelc S, Timperman I, Radisek S et al (2013) Comparative proteomic profiling in compatible and incompatible interactions between hop roots and Verticillium alboatrum. Plant Physiol Biochem 68:23–31PubMedCrossRefGoogle Scholar
  75. Maor R, Jones A, Nühse TS et al (2007) Multidimensional protein identification technology (MudPIT) analysis of ubiquitinated proteins in plants. Mol Cell Proteomics 6(4):601–610PubMedCrossRefGoogle Scholar
  76. Marouga R, David S, Hawkins E (2005) The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bio Anal Chem 382(3):669–678CrossRefGoogle Scholar
  77. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61PubMedCrossRefGoogle Scholar
  78. Mathesius U, Mulders S, Gao M et al (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci U S A 100:1444–1449PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mattinen L, Nissinen R, Riipi T et al (2007) Host-extract induced changes in the secretome of the plant pathogenic bacterium Pectobacterium atrosepticum. Proteomics 7:3527–3537PubMedCrossRefGoogle Scholar
  80. McGregor E, Dunn MJ (2006) Proteomics of the heart unraveling disease. Circ Res 98(3):309–321PubMedCrossRefGoogle Scholar
  81. Mehta A, Rosato YB (2001) Differentially expressed proteins in the interaction of Xanthomonas axonopodis pv. citri with leaf extract of the host plant. Proteomics 1:1111–1118PubMedCrossRefGoogle Scholar
  82. Mehta A, Brasileiro ACM, Souza DSL et al (2008) Plant–pathogen interactions: what is proteomics telling us? FEBS J 275:3731–3746PubMedCrossRefGoogle Scholar
  83. Meijer HJ, Van-de-Vondervoort PJ, Yin QY et al (2006) Identification of cell wall-associated proteins from Phytophthora ramorum. Mol Plant-Microbe Interact 19:1348–1358PubMedCrossRefGoogle Scholar
  84. Moore CD, Ajala OZ, Zhu H (2016) Applications in high-content functional protein microarrays. Curr Opin Chem Biol 30:21–27PubMedCrossRefGoogle Scholar
  85. Mukherjee AK, Carp MJ, Zuchman R et al (2010) Proteomics of the response of Arabidopsis thaliana to infection with Alternaria brassicicola. J Proteome 73:709–720CrossRefGoogle Scholar
  86. Mur LA, Kenton P, Lloyd AJ et al (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Expt Bot 59:501–520CrossRefGoogle Scholar
  87. Nat NVK, Srivastava S, Yajima W et al (2007) Application of proteomics to investigate plant-pathogen interactions. Curr Proteomics 4(1):28–43CrossRefGoogle Scholar
  88. Newton A, Fitt BDL, Atkins SD et al (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends Microbiol 18:365–373PubMedCrossRefGoogle Scholar
  89. Novak J, Lemr K, Schug KA et al (2015) CycloBranch: de novo sequencing of nonribosomal peptides from accurate product ion mass spectra. J Am Soc Mass Spectrom 10:1780–1786CrossRefGoogle Scholar
  90. Pakkianathan BC, Murad G (2014) Recent advances on interactions between the whitefly Bemisia tabaci and begomoviruses, with emphasis on Tomato yellow leaf curl virus. In: Gaur RK, Hohn T, Sharma P (eds) Plant virus-host interaction. Elsevier, Amsterdam, pp 79–103Google Scholar
  91. Perez-Bueno ML, Rahoutei J, Sajnani C et al (2004) Proteomic analysis of the oxygen evolving complex of photosystem II under biotic stress: studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4:418–425PubMedCrossRefGoogle Scholar
  92. Phalip V, Delalande F, Carapito C et al (2005) Diversity of the exoproteome of Fusarium graminearum grown on plant cell wall. Curr Genet 48:366–379PubMedCrossRefGoogle Scholar
  93. Pieterse CMJ, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 4:456–464CrossRefGoogle Scholar
  94. Rahoutei J, Baron M, Garcia-Luque I et al (1999) Effect of tobamovirus infection on the thermoluminescence characteristics of chloroplast from infected plants. Z Naturforsch Teil C 54:634–639Google Scholar
  95. Rahoutei J, Garcia-Luque I, Baron M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol Plant 110:286–292CrossRefGoogle Scholar
  96. Rampitsch C, Bykova NV, Mccallum B et al (2006) Analysis of the wheat and Puccinia triticina (leaf rust) proteomes during a susceptible host pathogen interaction. Proteomics 6:1897–1907PubMedCrossRefGoogle Scholar
  97. Righetti PG, Castagna A, Antonucci F et al (2004) Critical survey of quantitative proteomics in two-dimensional electrophoretic approaches. J Chromatogr A 1051:3–17PubMedCrossRefGoogle Scholar
  98. Rogowska-Wrzesinska A, Bihan MCL, Thaysen-Andersen M et al (2013) 2D gels still have a niche in proteomics. J Proteome 88:4–13CrossRefGoogle Scholar
  99. Romanov V, Davidoff SN, Miles AR et al (2014) A critical comparison of protein microarray fabrication technologies. Analyst 139(6):1303–1326PubMedCrossRefGoogle Scholar
  100. Rose JKC, Bashir S, Giovannoni JJ et al (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 5:715–733CrossRefGoogle Scholar
  101. Rosen R, Sacher A, Shechter N et al (2004) Two dimensional reference map of Agrobacterium tumefaciens proteins. Proteomics 4:1061–1073PubMedCrossRefGoogle Scholar
  102. Ross PL, Huang YN, Marchese JN et al (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3:1154–1169PubMedCrossRefGoogle Scholar
  103. Schenk PM, Choo JH, Wong CL (2009) Microarray analyses to study plant defense and rhizosphere microbe interaction. CAB Rev: Perspect Agric Vet Sci Nutr Nat Resour 45:1–14Google Scholar
  104. Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 63:451–482PubMedCrossRefGoogle Scholar
  105. Smith R (2009) Two-dimensional electrophoresis: an overview. In: Tyther R, Sheehan D (eds) Two-dimensional electrophoresis protocols. Humana Press, Totowa, pp 2–17CrossRefGoogle Scholar
  106. Speer R, Wulfkuhle JD, Liotta LA et al (2005) 3rd reverse-phase protein microarrays for tissue-based analysis. Curr Opin Mol Ther 7:240–245PubMedGoogle Scholar
  107. Speers AE, Wu CC (2007) Proteomics of integral membrane proteins theory and application. Chem Rev 107(8):3687–3714PubMedCrossRefGoogle Scholar
  108. Tanaka K, Waki H, Ido Y et al (1988) Protein and polymer analyses up to m/z 100,000 by laser ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 2:151–151CrossRefGoogle Scholar
  109. Tseng TT, Tyler BM, Setubal JC (2009) Protein secretion systems in bacterial-host associations, and their description in the gene ontology. BMC Microbiol 9:S2PubMedPubMedCentralCrossRefGoogle Scholar
  110. Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18:2071–2077PubMedCrossRefGoogle Scholar
  111. Vadivel AK (2015) Gel-based proteomics in plants: time to move on from the tradition. Front Plant Sci 6:369Google Scholar
  112. Valcu CM, Junqueira M, Shevchenko A (2009) Comparative proteomic analysis of responses to pathogen infection and wounding in Fagus sylvatica. J Proteome Res 8:4077–4091PubMedCrossRefGoogle Scholar
  113. Veenstra TD, Smith RD (eds) (2003) Proteome characterization and proteomics. Academic, San DiegoGoogle Scholar
  114. Ventelon-Debout M, Delalande F, Brizard JP et al (2004) Proteome analysis of cultivar-specific deregulations of Oryza sativa indica and O. sativa japonica cellular suspension undergoing rice yellow mottle virus infection. Proteomics 1:216–225CrossRefGoogle Scholar
  115. Wang L, Jiang W, Zhang Y et al (2013) Ax21-triggered immunity plays a significant role in rice defense against Xanthomonas oryzae pv. oryzicola. Phytopathology. https://doi.org/10.1094/PHYTO-12-12-0333-R
  116. Washburn MP, Wolters D, Yates JR (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19(3):242–247PubMedCrossRefGoogle Scholar
  117. Westermeier R (2006) Electrophoresis in practice. Wiley, WeinheimGoogle Scholar
  118. White IR, Pickford R, Wood J et al (2004) Statistical comparison of silver and SYPRO ruby staining for proteomic analysis. Electrophoresis 17:3048–3054CrossRefGoogle Scholar
  119. Wilkins MR, Sanchez JC, Gooley AA et al (1996) Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotechnol Genet Eng Rev 13:19–50PubMedCrossRefGoogle Scholar
  120. Wittmann-Liebold H, Graack HR, Pohl T (2006) Two dimensional gel electrophoresis as tool for proteomics studies in combination with protein identification by mass spectrometry. Proteomics 17:4688–4703CrossRefGoogle Scholar
  121. Yajima W, Kav NN (2006) The proteome of the phytopathogenic fungus Sclerotinia sclerotiorum. Proteomics 6:5995–6007PubMedCrossRefGoogle Scholar
  122. Yang F, Melo-Braga MN, Larsen MR et al (2013) Battle through signaling between wheat and the fungal pathogen Septoria tritici revealed by proteomics and phosphoproteomics. Mol Cell Proteomics 12:2497–2508PubMedPubMedCentralCrossRefGoogle Scholar
  123. Yang F, Li W, Derbyshire M et al (2015) Unraveling proteomics and Phosphoproteomics. Mol Cell Proteomics 12:2497–2508. incompatibility between wheat and the fungal pathogen Zymoseptoria tritici through apoplastic proteomics. BMC Genomics 16:362CrossRefGoogle Scholar
  124. Yates IJR, Gilchrist A, Howell KE et al (2005) Proteomics of organelles and large cellular structures. Nat Rev Mol Cell Biol 6(9):702–714PubMedCrossRefGoogle Scholar
  125. Zhou H, Ranish JA, Watts JD et al (2002) Quantitative proteome analysis by solid-phase isotope tagging and mass spectrometry. Nat Biotechnol 20(5):512–515PubMedCrossRefGoogle Scholar
  126. Zhou W, Eudes F, Laroche A (2006a) Identification of differentially regulated proteins in response to a compatible interaction between the pathogen Fusarium graminearum and its host, Triticum aestivum. Proteomics 6(16):4599–4609PubMedCrossRefGoogle Scholar
  127. Zhou W, Kolb FL, Riechers DE (2006b) Identification of proteins induced or upregulated by Fusarium head blight infection in the spikes of hexaploid wheat (Triticum aestivum). Genome 48(5):770–780CrossRefGoogle Scholar
  128. Zhu H, Bilgin M, Bangham R et al (2001) Global analysis of protein activities using proteome chips. Science 293:2101–2105PubMedCrossRefGoogle Scholar
  129. Zhu H, Bilgin M, Snyder M (2003) Proteomics. Annu Rev Biochem 1:783–812CrossRefGoogle Scholar
  130. Zhu W, Smith JW, Huang CM (2009) Mass spectrometry- based label-free quantitative proteomics. J Biomed Biotechnol 2010:Article ID: 840581Google Scholar
  131. Zhu M, Simons B, Zhu N et al (2010) Analysis of abscisic acid responsive proteins in brassica Napus guard cells by multiplexed isobaric tagging. J Proteome 73(4):790–805CrossRefGoogle Scholar
  132. Zhu N, Zhu M, Dai S et al (2012) An improved isotope-coded affinity tag technology for thiol redox proteomics. J Integr OMICS 2(1):17–23Google Scholar
  133. Zieske LR (2006) A perspective on the use of iTRAQ reagent technology for protein complex and profiling studies. J Exp Bot 57:1501–1508PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Anjana Rustagi
    • 1
  • Garvita Singh
    • 1
  • Shachi Agrawal
    • 1
  • Prem Kumar Gupta
    • 2
  1. 1.Department of BotanyGargi CollegeNew DelhiIndia
  2. 2.Ionics Clinical LaboratoryGurgaonIndia

Personalised recommendations