Looking deep Inside: Detection of low-abundance proteins in leaf extracts of Arabidopsis and phloem exudates of pumpkin

Plant Physiology

Volumn 159, Issue 3, 2012, Pages 902-914

  Fröhlich, Andreas ^a   Gaupels, Frank ^a   Sarioglu, Hakan ^a   Holzmeister, Christian ^a   Spannagl, Manuel ^a   Durner, Jörg ^a   Lindermayr, Christian ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); CUCURBITA MAXIMA; PSEUDOMONAS SYRINGAE;

EID: 84863643700     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.198077     Document Type: Article

References (77)

1. Ardales E, Moon S-J, Park DS Sr, Byun M-O, Noh TH (2009) Inactivation of argG, encoding argininosuccinate synthetase from Xanthomonas oryzae pv. oryzae, is involved in bacterial growth and virulence in planta. Can J Plant Pathol 31: 368-374.
2. Atkins CA, Smith PM, Rodriguez-Medina C (2011) Macromolecules in phloem exudates: a review. Protoplasma 248: 165-172.
3. Bachi A, Simó C, Restuccia U, Guerrier L, Fortis F, Boschetti E, Masseroli M, Righetti PG (2008) Performance of combinatorial peptide libraries in capturing the low-abundance proteome of red blood cells. 2. Behavior of resins containing individual amino acids. Anal Chem 80: 3557-3565.
4. Boschetti E, Lomas L, Citterio A, Righetti PG (2007) Romancing the "hidden proteome," Anno Domini two zero zero seven. J Chromatogr A 1153: 277-290.
5. Boschetti E, Righetti PG (2008a) Hexapeptide combinatorial ligand libraries: the march for the detection of the low-abundance proteome continues. Biotechniques 44: 663-665.
6. Boschetti E, Righetti PG (2008b) The ProteoMiner in the proteomic arena: a non-depleting tool for discovering low-abundance species. J Proteomics 71: 255-264.
7. Boschetti E, Righetti PG (2009) The art of observing rare protein species in proteomes with peptide ligand libraries. Proteomics 9: 1492-1510.
8. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, et al (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 100: 10181-10186.
9. Buettner JA, Dadd CA, Baumbach GA, Masecar BL, Hammond DJ (1996) Chemically derived peptide libraries: a new resin and methodology for lead identification. Int J Pept Protein Res 47: 70-83.
10. Castagna A, Cecconi D, Sennels L, Rappsilber J, Guerrier L, Fortis F, Boschetti E, Lomas L, Righetti PG (2005) Exploring the hidden human urinary proteome via ligand library beads. J Proteome Res 4: 1917-1930.
11. Cho WK, Chen XY, Rim Y, Chu H, Kim S, Kim SW, Park ZY, Kim JY (2010) Proteome study of the phloem sap of pumpkin using multidimensional protein identification technology. J Plant Physiol 167: 771-778.
12. Corthals GL, Wasinger VC, Hochstrasser DF, Sanchez JC (2000) The dynamic range of protein expression: a challenge for proteomic research. Electrophoresis 21: 1104-1115.
13. D'Amato A, Bachi A, Fasoli E, Boschetti E, Peltre G, Sénéchal H, Righetti PG (2009) In-depth exploration of cow's whey proteome via combinatorial peptide ligand libraries. J Proteome Res 8: 3925-3936.
14. D'Amato A, Bachi A, Fasoli E, Boschetti E, Peltre G, Sénéchal H, Sutra JP, Citterio A, Righetti PG (2010) In-depth exploration of Hevea brasiliensis latex proteome and "hidden allergens" via combinatorial peptide ligand libraries. J Proteomics 73: 1368-1380.
15. D'Amato A, Fasoli E, Kravchuk AV, Righetti PG (2011) Mehercules, adhuc Bacchus! The debate on wine proteomics continues. J Proteome Res 10: 3789-3801.
16. D'Amato A, Fasoli E, Righetti PG (2012) Harry Belafonte and the secret proteome of coconut milk. J Proteomics 75: 914-920.
17. D'Ambrosio C, Arena S, Scaloni A, Guerrier L, Boschetti E, Mendieta ME, Citterio A, Righetti PG (2008) Exploring the chicken egg white proteome with combinatorial peptide ligand libraries. J Proteome Res 7: 3461-3474.
18. Di Girolamo F, Boschetti E, Chung MC, Guadagni F, Righetti PG (2011) "Proteomineering" or not? The debate on biomarker discovery in sera continues. J Proteomics 74: 589-594.
19. Farinazzo A, Restuccia U, Bachi A, Guerrier L, Fortis F, Boschetti E, Fasoli E, Citterio A, Righetti PG (2009) Chicken egg yolk cytoplasmic proteome, mined via combinatorial peptide ligand libraries. J Chromatogr A 1216: 1241-1252.
20. Fasoli E, Aldini G, Regazzoni L, Kravchuk AV, Citterio A, Righetti PG (2010a) Les maîtres de l'orge: the proteome content of your beer mug. J Proteome Res 9: 5262-5269.
21. Fasoli E, D'Amato A, Citterio A, Righetti PG (2012) Ginger Rogers? No, ginger ale and its invisible proteome. J Proteomics 75: 1960-1965.
22. Fasoli E, D'Amato A, Kravchuk AV, Boschetti E, Bachi A, Righetti PG (2011a) Popeye strikes again: the deep proteome of spinach leaves. J Proteomics 74: 127-136.
23. Fasoli E, D'Amato A, Kravchuk AV, Citterio A, Righetti PG (2011b) Indepth proteomic analysis of non-alcoholic beverages with peptide ligand libraries. I. Almond milk and orgeat syrup. J Proteomics 74: 1080-1090.
24. Fasoli E, Farinazzo A, Sun CJ, Kravchuk AV, Guerrier L, Fortis F, Boschetti E, Righetti PG (2010b) Interaction among proteins and peptide libraries in proteome analysis: pH involvement for a larger capture of species. J Proteomics 73: 733-742.
25. Fito-Boncompte L, Chapalain A, Bouffartigues E, Chaker H, Lesouhaitier O, Gicquel G, Bazire A, Madi A, Connil N, Véron W, et al (2011) Full virulence of Pseudomonas aeruginosa requires OprF. Infect Immun 79: 1176-1186.
26. Fones H, Preston GM (2012) Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. FEMS Microbiol Lett 327: 1-8.
27. Fröhlich A, Lindermayr C (2011) Deep insights into the plant proteome by pretreatment with combinatorial hexapeptide ligand libraries. J Proteomics 74: 1182-1189.
28. Furka A, Sebestyén F, Asgedom M, Dibó G (1991) General method for rapid synthesis of multicomponent peptide mixtures. Int J Pept Protein Res 37: 487-493.
29. Garbom S, Forsberg A, Wolf-Watz H, Kihlberg BM (2004) Identification of novel virulence-associated genes via genome analysis of hypothetical genes. Infect Immun 72: 1333-1340.
30. Giavalisco P, Kapitza K, Kolasa A, Buhtz A, Kehr J (2006) Towards the proteome of Brassica napus phloem sap. Proteomics 6: 896-909.
31. Guerrier L, Claverol S, Finzi L, Paye F, Fortis F, Boschetti E, Housset C (2007a) Contribution of solid-phase hexapeptide ligand libraries to the repertoire of human bile proteins. J Chromatogr A 1176: 192-205.
32. Guerrier L, Claverol S, Fortis F, Rinalducci S, Timperio AM, Antonioli P, Jandrot-Perrus M, Boschetti E, Righetti PG (2007b) Exploring the platelet proteome via combinatorial, hexapeptide ligand libraries. J Proteome Res 6: 4290-4303.
33. Guerrier L, Thulasiraman V, Castagna A, Fortis F, Lin SH, Lomas L, Righetti PG, Boschetti E (2006) Reducing protein concentration range of biological samples using solid-phase ligand libraries. J Chromatogr B Analyt Technol Biomed Life Sci 833: 33-40.
34. Guo W, Cui YP, Li YR, Che YZ, Yuan L, Zou LF, Zou HS, Chen GY (2012) Identification of seven Xanthomonas oryzae pv. oryzicola genes potentially involved in pathogenesis in rice. Microbiology 158: 505-518.
35. Ha UH, Wang Y, Jin S (2003) DsbA of Pseudomonas aeruginosa is essential for multiple virulence factors. Infect Immun 71: 1590-1595.
36. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P, et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41: 1275-1281.
37. Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
38. Ibrahim YM, Kerr AR, Silva NA, Mitchell TJ (2005) Contribution of the ATP-dependent protease ClpCP to the autolysis and virulence of Streptococcus pneumoniae. Infect Immun 73: 730-740.
39. Jittawuttipoka T, Buranajitpakorn S, Vattanaviboon P, Mongkolsuk S (2009) The catalase-peroxidase KatG is required for virulence of Xanthomonas campestris pv. campestris in a host plant by providing protection against low levels of H2O2. J Bacteriol 191: 7372-7377.
40. Katagiri F, Thilmony R, He S (2002) The Arabidopsis thaliana-Pseudomonas syringae interaction. The Arabidopsis Book 1: e0039, doi/10.1199/tab.0039.
41. Keidel EM, Ribitsch D, Lottspeich F (2010) Equalizer technology: equal rights for disparate beads. Proteomics 10: 2089-2098.
42. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.
43. Kemner JM, Liang X, Nester EW (1997) The Agrobacterium tumefaciens virulence gene chvE is part of a putative ABC-type sugar transport operon. J Bacteriol 179: 2452-2458.
44. Kurth DG, Gago GM, de la Iglesia A, Lyonnet BB, Lin TW, Morbidoni HR, Tsai SC, Gramajo H (2009) ACCase 6 is the essential acetyl-CoA carboxylase involved in fatty acid and mycolic acid biosynthesis in mycobacteria. Microbiology 155: 2664-2675.
45. Lam KS, Salmon SE, Hersh EM, Hruby VJ, Kazmierski WM, Knapp RJ (1991) A new type of synthetic peptide library for identifying ligandbinding activity. Nature 354: 82-84.
46. Lamarche MG, Wanner BL, Crépin S, Harel J (2008) The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32: 461-473.
47. Li G, Nallamilli BR, Tan F, Peng Z (2008) Removal of high-abundance proteins for nuclear subproteome studies in rice (Oryza sativa) endosperm. Electrophoresis 29: 604-617.
48. Li H, Schenk A, Srivastava A, Zhurina D, Ullrich MS (2006) Thermoresponsive expression and differential secretion of the extracellular enzyme levansucrase in the plant pathogenic bacterium Pseudomonas syringae pv. glycinea. FEMS Microbiol Lett 265: 178-185.
49. Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
50. Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ (2009) Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics 8: 343-356.
51. Liu P, Wood D, Nester EW (2005) Phosphoenolpyruvate carboxykinase is an acid-induced, chromosomally encoded virulence factor in Agrobacterium tumefaciens. J Bacteriol 187: 6039-6045.
52. Malter D, Wolf S (2011) Melon phloem-sap proteome: developmental control and response to viral infection. Protoplasma 248: 217-224.
53. McEuen AR, Hill HAO (1982) Superoxide, hydrogen peroxide, and the gelling of phloem sap from Cucurbita pepo. Planta 154: 295-297.
54. McNairn E, Ni Bhriain N, Dorman CJ (1995) Overexpression of the Shigella flexneri genes coding for DNA topoisomerase IV compensates for loss of DNA topoisomerase I: effect on virulence gene expression. Mol Microbiol 15: 507-517.
55. Mehta A, Brasileiro AC, Souza DS, Romano E, Campos MA, Grossi-de-Sá MF, Silva MS, Franco OL, Fragoso RR, Bevitori R, et al (2008) Plantpathogen interactions: what is proteomics telling us? FEBS J 275: 3731-3746.
56. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, Goodman AL, Joachimiak G, Ordoñez CL, Lory S, et al (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526-1530.
57. Navarre WW, Zou SB, Roy H, Xie JL, Savchenko A, Singer A, Edvokimova E, Prost LR, Kumar R, Ibba M, et al (2010) PoxA, yjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol Cell 39: 209-221.
58. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658.
59. Peck SC (2005) Update on proteomics in Arabidopsis: where do we go from here? Plant Physiol 138: 591-599.
60. Preston GM (2000) Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol Plant Pathol 1: 263-275.
61. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, Ausubel FM (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
62. Righetti PG, Boschetti E (2008) The ProteoMiner and the FortyNiners: searching for gold nuggets in the proteomic arena. Mass Spectrom Rev 27: 596-608.
63. Rodriguez GM, Smith I (2006) Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J Bacteriol 188: 424-430.
64. Rose JK, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39: 715-733.
65. Roux-Dalvai F, Gonzalez de Peredo A, Simó C, Guerrier L, Bouyssié D, Zanella A, Citterio A, Burlet-Schiltz O, Boschetti E, Righetti PG, et al (2008) Extensive analysis of the cytoplasmic proteome of human erythrocytes using the peptide ligand library technology and advanced mass spectrometry. Mol Cell Proteomics 7: 2254-2269.
66. Schiano CA, Bellows LE, Lathem WW (2010) The small RNA chaperone Hfq is required for the virulence of Yersinia pseudotuberculosis. Infect Immun 78: 2034-2044.
67. Sen M, Shah B, Rakshit S, Singh V, Padmanabhan B, Ponnusamy M, Pari K, Vishwakarma R, Nandi D, Sadhale PP (2011) UDP-glucose 4,6-dehydratase activity plays an important role in maintaining cell wall integrity and virulence of Candida albicans. PLoS Pathog 7: e1002384.
68. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
69. Si Y, Yuan F, Chang H, Liu X, Li H, Cai K, Xu Z, Huang Q, Bei W, Chen H (2009) Contribution of glutamine synthetase to the virulence of Streptococcus suis serotype 2. Vet Microbiol 139: 80-88.
70. Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism: more than the icing on the cake. Plant J 61: 1067-1091.
71. Thulasiraman V, Lin S, Gheorghiu L, Lathrop J, Lomas L, Hammond D, Boschetti E (2005) Reduction of the concentration difference of proteins in biological liquids using a library of combinatorial ligands. Electrophoresis 26: 3561-3571.
72. Turgeon R, Oparka K (2010) The secret phloem of pumpkins. Proc Natl Acad Sci USA 107: 13201-13202.
73. Van Bel AJE, Gaupels F (2004) Pathogen-induced resistance and alarm signals in the phloem. Mol Plant Pathol 5: 495-504.
74. Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J (2004) Proteomics of cucurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65: 1795-1804.
75. Wharam SD, Mulholland V, Salmond GPC (1995) Conserved virulence factor regulation and secretion systems in bacterial pathogens of plants and animals. Eur J Plant Pathol 101: 1-13.
76. Zhang B, Tolstikov V, Turnbull C, Hicks LM, Fiehn O (2010) Divergent metabolome and proteome suggest functional independence of dual phloem transport systems in cucurbits. Proc Natl Acad Sci USA 107: 13532-13537.
77. Zhang C, Yu X, Ayre BG, Turgeon R (2012) The origin and composition of cucurbit "phloem" exudate. Plant Physiol 158: 1873-1882.