Modulation of protein phosphorylation, N-glycosylationand Lys-acetylation in grape (Vitis vinifera) mesocarp and exocarp owing to Lobesia botrana infection

Molecular and Cellular Proteomics

Volumn 11, Issue 10, 2012, Pages 945-956

  Melo Braga, Marcella N ^a   Verano Braga, Thiago ^a   León, Ileana R ^a   Antonacci, Donato ^b   Nogueira, Fábio C S ^a,c   Thelen, Jay J ^d   Larsen, Martin R ^a   Palmisano, Giuseppe ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPEPTIDE;

ACETYLATION; ARTICLE; GLYCOSYLATION; GRAPE; INFECTION; LOBESIA BOTRANA INFECTION; NONHUMAN; PLANT RESPONSE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; STEADY STATE; TANDEM MASS SPECTROMETRY;

ACETYLATION; AMINO ACID MOTIFS; ANIMALS; CHROMATOGRAPHY, LIQUID; FRUIT; GENE EXPRESSION REGULATION, PLANT; GLYCOSYLATION; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; MOTHS; PHOSPHOPEPTIDES; PHOSPHORYLATION; PLANT DISEASES; PLANT PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; STAINING AND LABELING; TANDEM MASS SPECTROMETRY; VITIS;

HEXAPODA; LOBESIA BOTRANA; MAMMALIA; VITACEAE; VITIS; VITIS VINIFERA;

EID: 84867176464     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.020214     Document Type: Article

References (63)

1. Jaillon, O., Aury, J. M., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Aubourg, S., Vitulo, N., Jubin, C., Vezzi, A., Legeai, F., Hugueney, P., Dasilva, C., Horner, D., Mica, E., Jublot, D., Poulain, J., Bruyère, C., Billault, A., Segurens, B., Gouyvenoux, M., Ugarte, E., Cattonaro, F., Anthouard, V., Vico, V., Del Fabbro, C., Alaux, M., Di Gaspero, G., Dumas, V., Felice, N., Paillard, S., Juman, I., Moroldo, M., Scalabrin, S., Canaguier, A., Le Clainche, I., Malacrida, G., Durand, E., Pesole, G., Laucou, V., Chatelet, P., Merdinoglu, D., Delledonne, M., Pezzotti, M., Lecharny, A., Scarpelli, C., Artiguenave, F., Pe, M. E., Valle, G., Morgante, M., Caboche, M., Adam-Blondon, A. F., Weissenbach, J., Quétier, F., and Wincker, P. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467 (Pubitemid 47509545)
2. Polesani, M., Bortesi, L., Ferrarini, A., Zamboni, A., Fasoli, M., Zadra, C., Lovato, A., Pezzotti, M., Delledonne, M., and Polverari, A. (2010) General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V. riparia) grapevine species. BMC Genomics 11, 117
3. Rotter, A., Camps, C., Lohse, M., Kappel, C., Pilati, S., Hren, M., Stitt, M., Coutos-Thevenot, P., Moser, C., Usadel, B., Delrot, S., and Gruden, K. (2009) Gene expression profiling in susceptible interaction of grapevine with its fungal pathogen Eutypa lata: extending MapMan ontology for grapevine. BMC Plant Biol. 9, 104
4. Chong, J., Le Henanff, G., Bertsch, C., and Walter, B. (2008) Identification, expression analysis and characterization of defense and signaling genes in Vitis vinifera. Plant Physiol. Biochem. 46, 469-481 (Pubitemid 351540849)
5. Milli, A., Cecconi, D., Bortesi, L., Persi, A., Rinalducci, S., Zamboni, A., Zoccatelli, G., Lovato, A., Zolla, L., and Polverari, A. (2012) Proteomic analysis of the compatible interaction between Vitis vinifera and Plasmopara viticola. J. Proteomics 75, 1284-1302
6. Giribaldi, M., Purrotti, M., Pacifico, D., Santini, D., Mannini, F., Caciagli, P., Rolle, L., Cavallarin, L., Giuffrida, M. G., and Marzachi, C. (2011) A multidisciplinary study on the effects of phloem-limited viruses on the agronomical performance and berry quality of Vitis vinifera cv. Nebbiolo. J. Proteomics 75, 306-315
7. Lin, H., Doddapaneni, H., Takahashi, Y., and Walker, M. A. (2007) Comparative analysis of ESTs involved in grape responses to Xylella fastidiosa infection. BMC Plant Biol. 7, 8
8. Ma, W., and Berkowitz, G. A. (2007) The grateful dead: calcium and cell death in plant innate immunity. Cell Microbiol. 9, 2571-2585 (Pubitemid 47500511)
9. Dangl, J. L., Dietrich, R. A., and Richberg, M. H. (1996) Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8, 1793-1807 (Pubitemid 27012405)
10. Ren, D., Liu, Y., Yang, K. Y., Han, L., Mao, G., Glazebrook, J., and Zhang, S. (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 105, 5638-5643 (Pubitemid 351753915)
11. Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gomez-Gomez, L., Boller, T., Ausubel, F. M., and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983 (Pubitemid 34193435)
12. Gleason, C., Huang, S., Thatcher, L. F., Foley, R. C., Anderson, C. R., Carroll, A. J., Millar, A. H., and Singh, K. B. (2011) Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl. Acad. Sci. U.S.A. 108, 10768-10773
13. Torres, M. A. (2010) ROS in biotic interactions. Physiol. Plant 138, 414-429
14. Yamada, T. (1993) The role of auxin in plant-disease development. Annu. Rev. Phytopathol. 31, 253-273
15. Gordon, D., Zahavi, T., Anshelevich, L., Harel, M., Ovadia, S., Dunkelblum, E., and Harari, A. R. (2005) Mating disruption of Lobesia botrana (Lepidoptera: Tortricidae): effect of pheromone formulations and concentrations. J. Econ. Entomol. 98, 135-142 (Pubitemid 40328474)
16. Cozzi, G., Pascale, M., Perrone, G., Visconti, A., and Logrieco, A. (2006) Effect of Lobesia botrana damages on black aspergilli rot and ochratoxin A content in grapes. Int. J. Food Microbiol. 111, Suppl 1, S88-92 (Pubitemid 44301562)
17. Vassiliou, V. A. (2011) Effectiveness of insecticides in controlling the first and second generations of the Lobesia botrana (Lepidoptera: Tortricidae) in table grapes. J. Econ. Entomol. 104, 580-585
18. Tasin, M., Bäckman, A. C., Bengtsson, M., Ioriatti, C., and Witzgall, P. (2006) Essential host plant cues in the grapevine moth. Naturwissenschaften 93, 141-144
19. Eichhorn, K. W., and Lorenz, H. (1977) Phaenologische Entwicklungstadien der Rebe. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes (Braunschweig) 29, 119-120
20. Isaacson, T., Damasceno, C. M., Saravanan, R. S., He, Y., Catalá, C., Saladie, M., and Rose, J. K. (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat. Protoc. 1, 769-774
21. Pinkse, M. W., Uitto, P. M., Hilhorst, M. J., Ooms, B., and Heck, A. J. (2004) Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns. Anal. Chem. 76, 3935-3943 (Pubitemid 38943662)
22. Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P., and Jørgensen, T. J. (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 4, 873-886 (Pubitemid 41309146)
23. Kuroda, I., Shintani, Y., Motokawa, M., Abe, S., and Furuno, M. (2004) Phosphopeptide-selective column-switching RP-HPLC with a titania precolumn. Anal. Sci. 20, 1313-1319
24. Engholm-Keller, K., Hansen, T. A., Palmisano, G., and Larsen, M. R. (2011) Multidimensional strategy for sensitive phosphoproteomics incorporating protein prefractionation combined with SIMAC, HILIC, and TiO(2) chromatography applied to proximal EGF signaling. J. Proteome Res. 10, 5383-5397
25. Mysling, S., Palmisano, G., Højrup, P., and Thaysen-Andersen, M. (2010) Utilizing ion-pairing hydrophilic interaction chromatography solid phase extraction for efficient glycopeptide enrichment in glycoproteomics. Anal. Chem. 82, 5598-5609
26. Palmisano, G., Melo-Braga, M. N., Engholm-Keller, K., Parker, B. L., and Larsen, M. R. (2012) Chemical deamidation: a common pitfall in large-scale N-linked glycoproteomic mass spectrometry-based analyses. J. Proteome Res. 11, 1949-1957
27. McNulty, D. E., and Annan, R. S. (2008) Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell. Proteomics 7, 971-980 (Pubitemid 351737096)
28. Palmisano, G., Lendal, S. E., Engholm-Keller, K., Leth-Larsen, R., Parker, B. L., and Larsen, M. R. (2010) Selective enrichment of sialic acid-containing glycopeptides using titanium dioxide chromatography with analysis by HILIC and mass spectrometry. Nat. Protoc. 5, 1974-1982
29. Rewitz, K. F., Larsen, M. R., Lobner-Olesen, A., Rybczynski, R., O'Connor, M. B., and Gilbert, L. I. (2009) A phosphoproteomics approach to elucidate neuropeptide signal transduction controlling insect metamorphosis. Insect Biochem. Mol. Biol. 39, 475-483
30. Schroeder, M. J., Shabanowitz, J., Schwartz, J. C., Hunt, D. F., and Coon, J. J. (2004) A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal. Chem. 76, 3590-3598 (Pubitemid 38868819)
31. Savitski, M. M., Lemeer, S., Boesche, M., Lang, M., Mathieson, T., Bantscheff, M., and Kuster, B. (2011) Confident phosphorylation site localization using the mascot delta score. Mol. Cell. Proteomics 10, 10.1074/mcp.M110.003830
32. Trelle, M. B., and Jensen, O. N. (2008) Utility of immonium ions for assignment of epsilon-N-acetyllysine-containing peptides by tandem mass spectrometry. Anal. Chem. 80, 3422-3430 (Pubitemid 351620730)
33. Conesa, A., Götz, S., Garcia-Gómez, J. M., Terol, J., Talón, M., and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676 (Pubitemid 41264107)
34. Gao, J., Agrawal, G. K., Thelen, J. J., and Xu, D. (2009) P3DB: a plant protein phosphorylation database. Nucleic Acids Res. 37, D960-962
35. Lerouge, P., Cabanes-Macheteau, M., Rayon, C., Fischette-Lainé, A. C., Gomord, V., and Faye, L. (1998) N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol. Biol. 38, 31-48 (Pubitemid 28403765)
36. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840
37. Finkemeier, I., Laxa, M., Miguet, L., Howden, A. J., and Sweetlove, L. J. (2011) Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis. Plant Physiol. 155, 1779-1790
38. Wu, X., Oh, M. H., Schwarz, E. M., Larue, C. T., Sivaguru, M., Imai, B. S., Yau, P. M., Ort, D. R., and Huber, S. C. (2011) Lysine acetylation is a widespread protein modification for diverse proteins in Arabidopsis. Plant Physiol. 155, 1769-1778
39. Schilling, B., Rardin, M. J., Maclean, B. X., Zawadzka, A. M., Frewen, B. E., Cusack, M. P., Sorensen, D. J., Bereman, M. S., Jing, E., Wu, C. C., Verdin, E., Kahn, C. R., Maccoss, M. J., and Gibson, B. W. (2012) Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in Skyline: application to protein acetylation and phosphorylation. Mol. Cell. Proteomics 11, 202-214
40. Sugiyama, N., Nakagami, H., Mochida, K., Daudi, A., Tomita, M., Shirasu, K., and Ishihama, Y. (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol. Syst. Biol. 4, 193
41. Nakagami, H., Sugiyama, N., Mochida, K., Daudi, A., Yoshida, Y., Toyoda, T., Tomita, M., Ishihama, Y., and Shirasu, K. (2010) Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol. 153, 1161-1174
42. Wang, Y., Nowak, G., Culley, D., Hadwiger, L. A., and Fristensky, B. (1999) Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica napus). MPMI 12, 410-418 (Pubitemid 29194711)
43. Ma, W., Smigel, A., Tsai, Y. C., Braam, J., and Berkowitz, G. A. (2008) Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulinlike protein. Plant Physiol. 148, 818-828 (Pubitemid 352847541)
44. Shimotohno, A., Umeda-Hara, C., Bisova, K., Uchimiya, H., and Umeda, M. (2004) The plant-specific kinase CDKF;1 is involved in activating phosphorylation of cyclin-dependent kinase-activating kinases in Arabidopsis. Plant Cell 16, 2954-2966 (Pubitemid 41075745)
45. Logemann, E., Wu, S. C., Schröder, J., Schmelzer, E., Somssich, I. E., and Hahlbrock, K. (1995) Gene activation by UV light, fungal elicitor or fungal infection in Petroselinum crispum is correlated with repression of cell cycle-related genes. Plant J. 8, 865-876 (Pubitemid 3009648)
46. Schwartz, D., and Gygi, S. P. (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398 (Pubitemid 41679391)
47. Adams, J. A. (2001) Kinetic and catalytic mechanisms of protein kinases. Chem. Rev. 101, 2271-2290
48. Reiland, S., Messerli, G., Baerenfaller, K., Gerrits, B., Endler, A., Grossmann, J., Gruissem, W., and Baginsky, S. (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol. 150, 889-903
49. Liu, C. C., Liu, C. F., Wang, H. X., Shen, Z. Y., Yang, C. P., and Wei, Z. G. (2011) Identification and analysis of phosphorylation status of proteins in dormant terminal buds of poplar. BMC Plant Biol. 11, 158
50. Edwards, A. V. G., Edwards, G. J., Larsen, M. R., and Cordwell, S. J. ReportSites - A computational method to extract positional and physicochemical information from large-scale proteomic post-translational modification datasets. J. Proteomics Bioinform. 5, 104-107
51. Schwartz, D., Chou, M. F., and Church, G. M. (2009) Predicting protein post-translational modifications using meta-analysis of proteome scale data sets. Mol. Cell. Proteomics 8, 365-379
52. Howe, G. A., and Jander, G. (2008) Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59, 41-66 (Pubitemid 351813023)
53. Sela-Buurlage, M. B., Ponstein, A. S., Bres-Vloemans, S. A., Melchers, L. S., Van Den Elzen, P., and Cornelissen, B. (1993) Only specific tobacco (Nicotiana tabacum) chitinases and [beta]-1,3-glucanases exhibit antifungal activity. Plant Physiol. 101, 857-863
54. Nürnberger, T., Brunner, F., Kemmerling, B., and Piater, L. (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198, 249-266 (Pubitemid 38406948)
55. Islam, M. A., Sturrock, R. N., Williams, H. L., and Ekramoddoullah, A. K. (2010) Identification, characterization, and expression analyses of class II and IV chitinase genes from Douglas-fir seedlings infected by Phellinus sulphurascens. Phytopathology 100, 356-366
56. Maurel, C., Verdoucq, L., Luu, D. T., and Santoni, V. (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu. Rev. Plant Biol. 59, 595-624 (Pubitemid 351813044)
57. Knight, M. R., Campbell, A. K., Smith, S. M., and Trewavas, A. J. (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352, 524-526
58. Boudsocq, M. (2010) [Plant calcium sensors in osmotic signaling]. Biol. Aujourdhui 204, 21-31
59. Zhu, S. Y., Yu, X. C., Wang, X. J., Zhao, R., Li, Y., Fan, R. C., Shang, Y., Du, S. Y., Wang, X. F., Wu, F. Q., Xu, Y. H., Zhang, X. Y., and Zhang, D. P. (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19, 3019-3036 (Pubitemid 350276709)
60. Zhao, R., Sun, H. L., Mei, C., Wang, X. J., Yan, L., Liu, R., Zhang, X. F., Wang, X. F., and Zhang, D. P. (2011) The Arabidopsis Ca(2+)-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol. 192, 61-73
61. Ludwig, A. A., Romeis, T., and Jones, J. D. (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J. Exp. Bot. 55, 181-188 (Pubitemid 38119160)
62. Kobayashi, M., Ohura, I., Kawakita, K., Yokota, N., Fujiwara, M., Shimamoto, K., Doke, N., and Yoshioka, H. (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065-1080 (Pubitemid 46953247)
63. Marsh, E., Alvarez, S., Hicks, L. M., Barbazuk, W. B., Qiu, W., Kovacs, L., and Schachtman, D. (2010) Changes in protein abundance during powdery mildew infection of leaf tissues of Cabernet Sauvignon grapevine (Vitis vinifera L.). Proteomics 10, 2057-2064