Label-free quantitative proteomics reveals differentially regulated proteins in the latex of sticky diseased Carica papaya L. plants

Journal of Proteomics

Volumn 75, Issue 11, 2012, Pages 3191-3198

  Rodrigues, Silas P ^a,b   Ventura, José A ^a,c   Aguilar, Clemente ^d   Nakayasu, Ernesto S ^d,e   Choi, HyungWon ^f   Sobreira, Tiago J P ^d   Nohara, Lilian L ^d   Wermelinger, Luciana S ^b   Almeida, Igor C ^d   Zingali, Russolina B ^b   Fernandes, Patricia M B ^a  

^a FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c Fazenda Experimental Bananal do Norte   (Brazil)

^d UNIVERSITY OF TEXAS AT EL PASO   (United States)

^e PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Carica papaya; Label free quantitative proteomics; Latex; Mass spectrometry; Plant proteomics

Indexed keywords

CHYMOPAPAIN; CYSTEINE PROTEINASE;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ELECTROSPRAY MASS SPECTROMETRY; ENZYMATIC ASSAY; NONHUMAN; PAPAYA; PAPAYA MELEIRA VIRUS; PLANT DISEASE; PLANT RESPONSE; PLANT VIRUS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; QUANTITATIVE ANALYSIS; STICKY SKIN; VIRUS INFECTION;

CARICA; PLANT DISEASES; PLANT PROTEINS; PLANT VIRUSES; PROTEOMICS;

CARICA PAPAYA;

EID: 84861672042     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.03.021     Document Type: Article

References (49)

1. Konno K. Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry 2011, 72(13):1510-1530.
2. Azarkan M., El Moussaoui A., van Wuytswinkel D., Dehon G., Looze Y. Fractionation and purification of the enzymes stored in the latex of Carica papaya. J Chromatogr B Analyt Technol Biomed Life Sci 2003, 790:229-238.
3. Konno K., Hirayama C., Nakamura M., Tateishi K., Tamura Y., Hattori M., et al. Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 2004, 37:370-378.
4. El Moussaoui A., Nijs M., Paul C., Wintjens R., Vincentelli J., Azarkan M., et al. Revisiting the enzymes stored in the laticifers of Carica papaya in the context of their possible participation in the plant defence mechanism. Cell Mol Life Sci 2001, 58:556-570.
5. Kitajima E.W., Rodrigues C., Silveira J., Alves F.L., Ventura J.A., Aragão F.J.L., et al. Association of isometric virus-like particles, restricted to laticifers, with "meleira" ("sticky disease") of papaya (Carica papaya). Fitopatol Bras 1993, 18:118-122.
6. Zambolim E.M., Alonso S.K., Matsuoka K.M., de Carvalho M.G., Zerbini F.M. Purification and some properties of Papaya meleira virus, a novel virus infecting papayas in Brazil. Plant Pathol 2003, 52:389-394.
7. Ventura J.A., Costa H., JdS Tatagiba Papaya diseases and integrated control. Diseases of fruits and vegetables: diagnosis and management 2004, 201-268. Klumer Academic Publishers, London. S.A.M.H. Naqvi (Ed.).
8. Rodrigues S.P., Da Cunha M., Ventura J.A., Fernandes P.M. Effects of the Papaya meleira virus on papaya latex structure and composition. Plant Cell Rep 2009, 28:861-871.
9. Cho W.K., Chen X.Y., Uddin N.M., Rim Y., Moon J., Jung J.H., et al. Comprehensive proteome analysis of lettuce latex using multidimensional protein-identification technology. Phytochemistry 2009, 70:570-578.
10. Rodrigues S.P., Ventura J.A., Aguilar C., Nakayasu E.S., Almeida I.C., Fernandes P.M., et al. Proteomic analysis of papaya (Carica papaya L.) displaying typical sticky disease symptoms. Proteomics 2011, 11:2592-2602.
11. Dielen A.S., Badaoui S., Candresse T., German-Retana S. The ubiquitin/26S proteasome system in plant-pathogen interactions: a never-ending hide-and-seek game. Mol Plant Pathol 2010, 11:293-308.
12. Lam E., Kato N., Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 2001, 411:848-853.
13. Thornberry N.A., Lazebnik Y. Caspases: enemies within. Science 1998, 281:1312-1316.
14. Woltering E.J. Death proteases come alive. Trends Plant Sci 2004, 9:469-472.
15. Gilroy E.M., Hein I., van der Hoorn R., Boevink P.C., Venter E., McLellan H., et al. Involvement of cathepsin B in the plant disease resistance hypersensitive response. Plant J 2007, 52:1-13.
16. Moutim V., Silva L.G., Lopes M.T.P., Fernandes G.W., Salas C.E. Spontaneous processing of peptides during coagulation of latex from Carica papaya. Plant Sci 1999, 142:115-121.
17. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
18. Rodrigues S.P., Andrade J.S., Ventura J.A., Lindsey G.G., Fernandes P.M.B. Papaya meleira virus is neither transmitted by infection at wound sites nor by the whitefly Trialeurodes variabilis. J Plant Pathol 2009, 1:87-91.
19. Araujo M.M., Tavares E.T., Silva F.R., Marinho V.L., Junior M.T. Molecular detection of Papaya meleira virus in the latex of Carica papaya by RT-PCR. J Virol Methods 2007, 146:305-310.
20. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
21. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
22. Neuhoff V., Arold N., Taube D., Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 1988, 9:255-262.
23. Rodrigues S.P., Ventura J.A., Zingali R.B., Fernandes R.M.B. Evaluation of sample preparation methods for the analysis of papaya leaf proteins through two-dimensional gel electrophoresis. Phytochem Anal 2009, 20:456-464.
24. Cui S., Hu J., Yang B., Shi L., Huang F., Tsai S.N., et al. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 1994, 5:976-989.
25. Nakayasu E.S., Sobreira T.J., Torres R., Ganiko L., Oliveira P.S., Marques A.F., et al. Improved proteomic approach for the discovery of potential vaccine targets in Trypanosoma cruzi. J Proteome Res 2011, 11(1):237-246.
26. Peng J., Elias J.E., Thoreen C.C., Licklider L.J., Gygi S.P. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2003, 2:43-50.
27. Polpitiya A.D., Qian W.J., Jaitly N., Petyuk V.A., Adkins J.N., Camp D.G., et al. DAnTE: a statistical tool for quantitative analysis of -omics data. Bioinformatics 2008, 24:1556-1558.
28. Choi H., Fermin D., Nesvizhskii A.I. Significance analysis of spectral count data in label-free shotgun proteomics. Mol Cell Proteomics 2008, 7:2373-2385.
29. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
30. Pande M., Dubey V.K., Yadav S.C., Jagannadham M.V. A novel serine protease cryptolepain from Cryptolepis buchanani: purification and biochemical characterization. J Agric Food Chem 2006, 54:10141-10150.
31. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009, 6:359-362.
32. Song I., Taylor M., Baker K., Bateman R.C. Inhibition of cysteine proteinases by Carica papaya cystatin produced in Escherichia coli. Gene 1995, 162:221-224.
33. Manners D.J., Wilson G. Purification and properties of an endo-(1 leads to 3)-beta-d-glucanase from malted barley. Carbohydr Res 1974, 37:9-22.
34. Dhouib R., Laroche-Traineau J., Shaha R., Lapaillerie D., Solier E., Ruales J., et al. Identification of a putative triacylglycerol lipase from papaya latex by functional proteomics. FEBS J 2011, 278:97-110.
35. Barrett A.J., Kembhavi A.A., Brown M.A., Kirschke H., Knight C.G., Tamai M., et al. l-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L. Biochem J 1982, 201:189-198.
36. Azarkan M., Dibiani R., Baulard C., Baeyens-Volant D. Effects of mechanical wounding on Carica papaya cysteine endopeptidases accumulation and activity. Int J Biol Macromol 2006, 38:216-224.
37. Pickard W.F. Laticifers and secretory ducts: two other tube systems in plants. New Phytol 2008, 177:877-888.
38. Larosa P.C., Chen Z., Nelson D.E., Singh N.K., Hasegawa P.M., Bressan R.A. Osmotin gene expression is posttranscriptionally regulated. Plant Physiol 1992, 100:409-415.
39. Dorokhov Y.L., Makinen K., Frolova O.Y., Merits A., Saarinen J., Kalkkinen N., et al. A novel function for a ubiquitous plant enzyme pectin methylesterase: the host-cell receptor for the tobacco mosaic virus movement protein. FEBS Lett 1999, 461:223-228.
40. Dorokhov Y.L., Frolova O.Y., Skurat E.V., Ivanov P.A., Gasanova T.V., Sheveleva A.A., et al. A novel function for a ubiquitous plant enzyme pectin methylesterase: the enhancer of RNA silencing. FEBS Lett 2006, 580:3872-3878.
41. Yang D.H., Hettenhausen C., Baldwin I.T., Wu J. BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata's responses to herbivory. J Exp Bot 2011, 62:641-652.
42. van der Hoorn R.A. Plant proteases: from phenotypes to molecular mechanisms. Annu Rev Plant Biol 2008, 59:191-223.
43. Xu Q.F., Cheng W.S., Li S.S., Li W., Zhang Z.X., Xu Y.P., et al. Identification of genes required for Cf-dependent hypersensitive cell death by combined proteomic and RNA interfering analyses. J Exp Bot 2012, 10.1093/jxb/err397.
44. Solomon M., Belenghi B., Delledonne M., Menachem E., Levine A. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 1999, 11:431-444.
45. Rooney H.C. Van't Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 2005, 308:1783-1786.
46. Tian M., Win J., Song J., van der Hoorn R., van der Knaap E., Kamoun S. A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol 2007, 143:364-377.
47. Nagy P.D., Wang R.Y., Pogany J., Hafren A., Makinen K. Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 2011, 411:374-382.
48. Chen Z., Zhou T., Wu X., Hong Y., Fan Z., Li H. Influence of cytoplasmic heat shock protein 70 on viral infection of Nicotiana benthamiana. Mol Plant Pathol 2008, 9:809-817.
49. Kanzaki H., Saitoh H., Ito A., Fujisawa S., Kamoun S., Katou S., et al. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol Plant Pathol 2003, 4:383-391.