Changes in the proteome of pad2-1, a glutathione depleted Arabidopsis mutant, during Pseudomonas syringae infection

Journal of Proteomics

Volumn 126, Issue , 2015, Pages 82-93

  Datta, Riddhi ^a   Chattopadhyay, Sharmila ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

GSH; Infection; Pad2 1; Proteomics; Pseudomonas syringae

Indexed keywords

GLUTATHIONE; GLUTATHIONE TRANSFERASE; GLYCINE RICH REPEAT RNA BINDING PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 17; LEUCINE RICH REPEAT RECEPTOR KINASE; PROTEIN; PROTEIN PAD2 1; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; PROTEOME;

ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; INFECTION SENSITIVITY; NONHUMAN; NUCLEOTIDE BINDING SITE; PATHOGENESIS; PLANT DEFENSE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEOMICS; PSEUDOMONAS INFECTION; PSEUDOMONAS SYRINGAE INFECTION; WILD TYPE; ARABIDOPSIS; DISEASE RESISTANCE; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PLANT DISEASE; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DISEASE RESISTANCE; GLUTATHIONE; MUTATION; PLANT DISEASES; PROTEOME; PSEUDOMONAS SYRINGAE;

EID: 84930938095     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.04.036     Document Type: Article

References (63)

1. Food and Agricultural Organization of the United Nations, FAO Plant pests and diseases Available at:. http://www.fao.org/emergencies/emergency-types/plant-pests-and-diseases/en/.
2. Chakraborty S., Newton A.C. Climate change, plant diseases and food security: an overview. Plant Pathol. 2011, 60:2-14.
3. Boller T., Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009, 60:379-406.
4. Ingle R.A., Carstens M., Denby K.J. PAMP recognition and the plant pathogen arms race. BioEssays 2006, 28:880-889.
5. Lipka V., Dittgen J., Bednarek P., Bhat R., Wiermer M., Stein M., Landtaq J., Brandt W., Roshal S., Scheel D., Liorente F., Molina A., Parker J., Somervile S., Schulze-lefert P. Pre- and post-invasion defences both contribute to non-host resistance in Arabidopsis. Science 2005, 310:1180-1183.
6. Chisholm S.T., Coaker G., Day B., Staskawicz B.J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124:803-814.
7. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
8. Zipfel C. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 2008, 20:10-16.
9. Mukherjee A.K., Carp M.J., Zuchman R., Ziv T., Horwitza B.A., Gepstein S. Proteomics of the response of Arabidopsis thaliana to infection with Alternaria brassicicola. J. Proteome 2010, 73:709-720.
10. Noctor G., Gomez L., Vanacker H., Foyer C.H. Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J. Exp. Bot. 2002, 53:1283-1304.
11. Ball L., Accotto G.P., Bechtold U., Creissen G., Funck D., Jimenez A., Kular B., Leyland N., Mejia-Carranza J., Reynolds H., Karpinski S., Mullineaux P.M. Evidence for a direct link between glutathione biosynthesis and stress defence gene expression in Arabidopsis. Plant Cell 2004, 16:2448-2462.
12. Ishikawa K., Yoshimura K., Harada K., Fukusaki E., Ogawa T., Tamoi M., Shiqeoka S. AtNUDX6, an ADP-ribose/NADH pyrophosphohydrolase in Arabidopsis positively regulates NPR1-dependent salicylic acid signalling. Plant Physiol. 2010, 152:2000-2012.
13. Lim B., Pasternak M., Meyer A.J., Cobbett C.S. Restricting glutamyl cysteine synthetase activity to the cytosol or glutathione biosynthesis to the plastid is sufficient for normal plant development and stress tolerance. Plant Biol. 2014, 16:58-67.
14. Dron M., Clouse S.D., Dixon R.A., Lawton M.A., Lamb C.J. Glutathione and fungal elicitor regulation of a plant defence gene promoter in electroporated protoplasts. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:6738-6742.
15. Wingate V.P.M., Lawton M.A., Lamb C.J. Glutathione causes a massive and selective induction of plant defence genes. Plant Physiol. 1988, 87:206-210.
16. Parisy V., Poinssot B., Owsianowski L., Buchala A., Glazebrook J., Mauch F. Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J. 2007, 49:159-172.
17. Frendo P., Baldacci-Cresp F., Benyamina S.M., Puppo A. Glutathione and plant response to the biotic environment. Free Radic. Biol. Med. 2013, 65:724-730.
18. Dubreuil-Maurizi C., Poinssot B. Role of glutathione in plant signaling under biotic stress. Plant Signal. Behav. 2012, 7:210-212.
19. Kumar D., Datta R., Hazra S., Sultana A., Mukhopadhyay R., Chattopadhyay S. Transcriptomic profiling of Arabidopsis thaliana mutant pad2.1 in response to combined cold and osmotic stress. PLoS ONE 2015, 10:e0122690.
20. Mittova V., Theodoulou F.L., Kiddle G., Gomez L., Volokita M., Tal M., Foyer C.H., Guy M. Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett. 2003, 554:417-421.
21. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 1994, 79:583-593.
22. Ghanta S., Bhattacharyya D., Sinha R., Banerjee A., Chattopadhyay S. Nicotiana tabacum overexpressing γ-ECS exhibits biotic stress tolerance likely through NPR1-dependent salicylic acid-mediated pathway. Planta 2011, 233:895-910.
23. Ghanta S., Bhattacharyya D., Chattopadhyay S. Glutathione signaling acts through NPR1-dependent SA-mediated pathway to mitigate biotic stress. Plant Signal. Behav. 2011, 6:607-609.
24. 2 to activation of salicylic acid accumulation and signaling. Antioxid. Redox Signal. 2013, 18:2106-2121.
25. Ghanta S., Datta R., Bhattacharyya D., Sinha R., Kumar D., Hazra S., Mazumdar A.B., Chattopadhyay S. Multistep involvement of glutathione with salicylic acid and ethylene to combat environmental stress. J. Plant Physiol. 2014, 171:940-950.
26. Jorrin-Novo J.V., Pascual J., Lucas R.S., Romero-Rodriguez C., Ortega M.R., Lenz C., Valledor L. Fourteen years of plant proteomics reflected in Proteomics: Moving from model species and 2-DE based approaches to orphan species and gel-free platforms. Proteomics 2015, 15:1089-1112.
27. Mehta A., Brasileiro A.C., Souza D.S., Romano E., Campos M.A., Grossi-de-Sa M.F., Silva M.S., Franco O.L., Fraqosso R.R., Bevitori R., Rocha T.L. Plant-pathogen interactions: what is proteomics telling us?. FEBS J. 2008, 275:3731-3746.
28. Wu L., Han Z., Wang S., Wang X., Sun A., Zu X., Chen Y. Comparative proteomic analysis of the plant-virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. J. Proteome 2013, 89:124-140.
29. Petriccione M., Cecco I.D., Arena S., Scaloni A., Scortichini M. Proteomic changes in Actinidia chinensis shoot during systemic infection with a pandemic Pseudomonas syringae pv. actinidiae strain. J. Proteome 2013, 78:461-476.
30. Hirano S.S., Upper C.D. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 2000, 64:624-653.
31. Jones A.M., Thomas V., Truman B., Lilley K., Mansfield J., Grant M. Specific changes in the Arabidopsis proteome in response to bacterial challenge: differentiating basal and R-gene mediated resistance. Phytochemistry 2004, 65:1805-1816.
32. Sappl P.G., Onate-Sanchez L., Singh K.B., Millar A.H. Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Mol. Biol. 2004, 54:205-219.
33. Datta R., Sinha R., Chattopadhyay S. Changes in leaf proteome profile of Arabidopsis thaliana in response to salicylic acid. J. Biosci. 2013, 38:1-12.
34. Dong X., Mindrinos M., Davis K.R., Ausubel F.M. Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 1991, 3:61-72.
35. Pozo M.J., Van der Ent S., Van Loon L.C., Pieterse C.M. Transcription factor MYC2 is involved in priming for enhanced defence during rhizobacteria induced systemic resistance in Arabidopsis thaliana. New Phytol. 2008, 180:511-523.
36. Lichtenthaler H.K. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 1987, 148:350-382.
37. Isaacson T., Damasceno C.M.B., Saravanan R.S., He Y., Catala C., Saladié M., Rose J.K. Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat. Protoc. 2006, 1:769-774.
38. Sinha R., Chattopadhyay S. Changes in the leaf proteome profile of Mentha arvensis in response to Alternaria alternata infection. J. Proteome 2011, 74:327-336.
39. 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.
40. 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.
41. Kanehisa M., Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000, 28:27-30.
42. Bjellqvist B., Hughes G.J., Pasquali C., Paquet N., Ravier F., Sanchez J.C., Frutiger S., Hochstrasser D. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 1993, 14:1023-1031.
43. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M.R., Appel R.D., Bairoch A. Protein identification and analysis tools on the ExPASy server. The Proteomics Protocols Handbook 2005, 571-607. Humana Press. J.M. Walker (Ed.).
44. Valledor L., Jorrín J. Back to the basics: Maximizing the information obtained by quantitative two dimensional gel electrophoresis analyses by an appropriate experimental design and statistical analyses. J. Proteome 2011, 74:1-18.
45. DeYoung B.J., Innes R.W. Plant NBS-LRR proteins in pathogen sensing and host defence. Nat. Immunol. 2006, 7:1243-1249.
46. Torii K.U. Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int. Rev. Cytol. 2004, 234:1-46.
47. Sun W., Bernard C., van de Cotte B., Van Montagu M., Verbruggen N. At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J. 2001, 27:407-415.
48. Kim J.S., Park S.J., Kwak K.J., Kim Y.O., Kim J.Y., Song J., Jang B., Jung C.-H., Kang H. Cold shock domain proteins and glycine rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in E. coli. Nucleic Acids Res. 2007, 35:506-516.
49. Chen J.-H., Jiang H.-W., Hsieh E.-J., Chen H.-Y., Chien C.-T., Hsieh H.-L., Lin T.-P. Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol. 2012, 158:340-351.
50. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 2010, 11:539-548.
51. Jorrin-Novo J.V., Maldonado A.M., Echevarria-Zomeno S., Valledor L., Castillejo M.A., Curto M., Valero J., Sqhaier B., Donoso G., Redondo I. Plant proteomics update (2007-2008): second-generation proteomic techniques, an appropriate experimental design, and data analysis to fulfill MIAPE standards, increase plant proteome coverage and expand biological knowledge. J. Proteome 2009, 72:285-314.
52. Link G. Green life: Control of chloroplast gene transcription. BioEssays 1996, 18:465-471.
53. Roux M., Schwessinger B., Albrecht C., Chinchilla D., Jones A., Holton N., Malinovsky F.G., Tör M., de Vries S., Zipfel C. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 2011, 23:2440-2455.
54. Kang Y.J., Kim K.H., Shim S., Yoon M.Y., Sun S., Kim M.Y., Van K., Lee S.H. Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol. 2012, 12:139.
55. Katiyar A.L., Smita S., Lenka S.K., Rajwanshi R., Chinnusamy V., Bansal K.C. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 2012, 10:544.
56. Sinha R., Kumar D., Datta R., Hazra S., Bhattacharyya D., Majumdar A.B., Mukhopadhyay R., Sultana A., Chattopadhyay S. Integrated transcriptomic and proteomic analysis of Arabidopsis thaliana exposed to glutathione unravels its role in plant defence. Plant Cell Tissue Organ Cult. 2015, 120:975-988.
57. Kim J.Y., Kim W.Y., Kwak K.J., Oh S.H., Han Y.S., Kang H. Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process. J. Exp. Bot. 2010, 61:2317-2325.
58. Chi Y., Cheng Y., Vanitha J., Kumar N., Ramamoorthy R., Ramachandran S., Jiang S.Y. Expansion mechanisms and functional divergence of the glutathione S-transferase family in Sorghum and other higher plants. DNA Res. 2011, 18:1-16.
59. Zagorchev L., Seal C.E., Kranner I., Odjakova M. A central role for thiols in plant tolerance to abiotic stress. Int. J. Mol. Sci. 2013, 14:7405-7432.
60. Swindell W.R., Huebner M., Weber A.P. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 2007, 8:125.
61. Chandran D., Inadaa N., Hatherb G., Kleindtc C.K., Wildermuth M.C. Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:460-465.
62. Wan X.Y., Liu J.Y. Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves. Mol. Cell. Proteomics 2008, 7:1469-1488.
63. Weiss W., Gorg A. Two-dimensional electrophoresis for plant proteomics. Methods Mol. Biol. 2007, 355:121-143.