A proteomic approach analysing the Arabidopsis thaliana response to virulent and avirulent Pseudomonas syringae strains

• Autorzy: Sghaier-Hammami B. , Redondo-Lopez I. , Maldonado-Alconada A. M. , Echevarria-Zomeno S. , Jorrin-Novo J. V.
• Języki publikacji: EN

Abstrakty

EN

The present work is directed at studying changes at the proteome level in Arabidopsis thaliana leaves in response to Pseudomonas syringae virulent (Pst) and avirulent (Pst avrRpt2) strains. Arabidopsis leaves were sampled from challenged plants at 4, 8 and 24 h post inoculation. Proteins were TCA–acetone–phenol extracted and subjected to 2-DE (5–8 pH range) and MS/MS (MALDI–TOF–TOF) analysis. Out of 800 matched spots on each of the 36 gels analysed, 147 spots were either absent in at least one of the conditions studied (time or treatments; qualitative variable spots) or differentially accumulated between time and treatments (quantitative variable spots). Out of the 24 proteins successfully identified over TAIR10 database, 23 have not been reported previously in similar proteomics studies of the Arabidopsis thaliana–Pseudomonas syringae interaction. The exhaustive statistical analysis performed, including principal component and heat map, showed that 24 h post inoculation can clearly discriminate the challenged plants from the control. The protein change occurred early (4 h post inoculation) following the virulent pathogen infection, whereas the change occurred later (24 h post inoculation) following the avirulent pathogen inoculation. Concerning the variable proteins, three behavioural groups can be observed: group 1 (common protein changes in response to virulent and avirulent pathogen infection), group 2 (protein changes in response to virulent pathogen infection) and group 3 (protein changes in response to avirulent pathogen infection). Differential identified proteins following the pathogen infection belonged to different groups including those of oxidative stress defence, enzymes of metabolic pathways and molecular chaperones.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2012
• Tom: 34
• Numer: 3
• Opis fizyczny: p.905-922,fig.,ref.

Twórcy

autor

Sghaier-Hammami B.

• Department of Biochemistry and Molecular Biology, Agricultural and Plant Biochemistry and Proteomics Research Group, University of Cordoba, Campus de Rabanales, Ed. Severo Ochoa (C6), 14071 Cordoba, Spain

autor

Redondo-Lopez I.

• Department of Biochemistry and Molecular Biology, Agricultural and Plant Biochemistry and Proteomics Research Group, University of Cordoba, Campus de Rabanales, Ed. Severo Ochoa (C6), 14071 Cordoba, Spain

autor

Maldonado-Alconada A. M.

• Department of Biochemistry and Molecular Biology, Agricultural and Plant Biochemistry and Proteomics Research Group, University of Cordoba, Campus de Rabanales, Ed. Severo Ochoa (C6), 14071 Cordoba, Spain

autor

Echevarria-Zomeno S.

• Department of Biochemistry and Molecular Biology, Agricultural and Plant Biochemistry and Proteomics Research Group, University of Cordoba, Campus de Rabanales, Ed. Severo Ochoa (C6), 14071 Cordoba, Spain

autor

Jorrin-Novo J. V.

• Department of Biochemistry and Molecular Biology, Agricultural and Plant Biochemistry and Proteomics Research Group, University of Cordoba, Campus de Rabanales, Ed. Severo Ochoa (C6), 14071 Cordoba, Spain

Bibliografia

• Bashan Y, Sharon E, Okon Y, Henis Y (1981) Scanning electron and light microscopy of infection and symptom development in tomato leaves infected with Pseudomonas tomato. Physiol Plant Pathol 19:139–144
• Carrari F, Nunes-Nesi A, Gibon Y, Lytovchenko A, Ehlers-Loureiro M, Fernie AR (2003) Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiol 133:1322–1335
• Chich JF, David O, Villers F, Schaeffer B, Lutomski D, Huet S (2007) Statistics for proteomics: experimental design and 2-DE differential analysis. J Chromatogr B 849:261–272
• Chivasa S, Hamilton JM, Pringle RS, Ndimba BK, Simon WJ, Lindsey K, Slabas AR (2006) Proteomic analysis of differentially expressed proteins in fungal elicitor-treated Arabidopsis cell cultures. J Exp Bot 57:1553–1562
• Cho MS, Shin SH, Kim KS, Kim YC, Eun MY, Cho BH (2004) Enhanced expression of a gene encoding a nucleoside diphosphate kinase 1 (OsNDPK1) in rice plants upon infection with bacterial pathogens. Mol Cells 18:390–395
• Cobbett CS, May MJ, Howden R, Rolls B (1998) The glutathionedeficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in g-glutamylcysteine synthetase. Plant J 16:73–78
• Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR (2002) Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol 10:462–469
• Cornels H, Ichinose Y, Barz W (2000) Characterization of cDNAs encoding two glycine-rich proteins in chickpea (Cicer arietinum L.): accumulation in response to fungal infection and other stress factors. Plant Sci 154:83–88
• Cuppels DA (1986) Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl Environ Microbiol 51:323–327
• Dangl JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833
• De Vienne D, Bost B, Fiévet J, Zivy M, Dillmann C (2001) Genetic variability of proteome expression and metabolic control. Plant Physiol Biochem 39:271–283
• Desimone M, Wagner E, Johanningmeier U (1998) ATP-dependent proteolytic activity of chloroplasts degrades active oxygen modified ribulose 1,5-biphophate carboxylase/oxygenase. Planta 205:459–466
• Dong X, Mindrinos M, Davis KR, Ausubel FM (1991) Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3:61–72
• Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868
• Fang RX, Pang Z, Gao DM, Mang KG, Chua NH (1991) cDNA sequence of a virus-inducible, glycine-rich protein gene from rice. Plant Mol Biol 17:1255–1257
• Finnie C, Bak-Jensen KS, Laugesen S, Roepstorff P, Svensson B (2006) Differential appearance of isoforms and cultivar variation in protein temporal profiles revealed in the maturing barley grain proteome. Plant Sci 170:808–821
• Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signalling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
• Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organization of Arabidopsis leaves. Plant J 33:691–705
• Ge X, Li GJ,Wang SB, ZhuH,Zhu T,Wang X, XiaY(2007) AtNUDT7, a negative regulator of basal immunity in Arabidopsis, modulates two distinct defense response pathways and is involved in maintaining redox homeostasis. Plant Physiol 145:204–215
• Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW,Dangl JL (1995) Structure of the ArabidopsisRPM1gene which enables dual-specificity disease resistance. Science 269:843–846
• Gustafsson JS, Robert C, Glasbey CA, Blomberg A, Rudemo M (2004) Statistical exploration of variation in quantitative twodimensional gel electrophoresis data. Proteomics 4:3791–3799
• Ishida H, Shimizu S, Makino A, Mae T (1998) Light-dependent fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts isolated from wheat leaves. Planta 204:305–309
• Ishida H, Makino A, Mae T (1999) Fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase by reactive oxygen species occurs near Gly-329. J Biol Chem 274:5222–5226
• Jacobsen S, Grove H, Jensen KN, Sørensen HA et al (2007) Multivariate analysis of 2-DE protein patterns—practical approaches. Electrophoresis 28:1289–1299
• Jambunathan N, Penaganti A, Tang Y, Mahalingam R (2010) Modulation of redox homeostasis under suboptimal conditions by Arabidopsis nudix hydrolase 7. BMC Plant Biol 10:173. doi: 10.1186/1471-2229-10-173
• Jelitto-Van DEP, Vidal S, Denecke J (1999) Anticipating endoplasmic reticulum stress: a novel early response before pathogenesisrelated gene induction. Plant Cell 11:1935–1943
• Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
• Jones AM, Thomas V, Truman B, Lilley K, Mansfield J, Grant M (2004) Specific changes in the Arabidopsis proteome in response to bacterial challenge: differentiating basal and R-gene mediated resistance. Phytochem 65:1805–1816
• Jones AME, Thomas V, Bennett MH, Mansfield J, Grant M (2006) Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol 142:1603–1620
• Jorge I, Navarro RM, Lenz C, Ariza D, Porras C, Jorrin J (2005) The holm oak leaf proteome: analytical and biological variability in the protein expression level assessed by 2-DE and protein identification tandem mass spectrometry de novo sequencing and sequence similarity searching. Proteomics 5:222–234
• Jorrín-Novo JV, Maldonado AM, Echevarría-Zomeño S, Valledor L, Castillejo MA, Curto M, Valero J, Sghaier B, Donoso G, Redondo I (2009) Plant proteomics update (2007–2008): secondgeneration proteomic techniques, an appropriate experimental. J Proteomics 72:285–314
• Kelly BS, Antholine WE, Griffith OW (2002) Escherichia coli gamma-glutamylcysteine synthetase. Two active site metal ions affect substrate and inhibitor binding. Biol Chem 277:50–58
• Kim MG, Kim SY, Kim WY, Mackey D, Lee SY (2008) Responses of Arabidopsis thaliana to challenge by Pseudomonas syringae. Mol Cells 25:323–331
• Kimura Y, Yahara I, Lindquist S (1995) Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science 268:1362–1365
• King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocianin and fluorescein. JLab ClinMed 44:301–307
• Kohler G, Linkert C, Barz W (1995) Infection Studies of Cicer arietinum (L.) with GUS-(E. coli b-glucuronidase) transformed Ascochyta rabiei strains. J Phytopathol 143:589–595
• Laemmli UK (1979) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685
• Lam E, Kato N, LawtonM(2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853
• Leelavathi S, Bhardwaj A, Kumar S, Dass A, Pathak R, Pandey SS, Tripathy BC, Padmalatha KV, Dhandapani G, Kanakachari M, Kumar PA, Cella R, Reddy SV (2011) Genome-wide transcriptome and proteome analyses of tobacco psaA and psbA deletion mutants. Plant Mol Biol 76:407–423
• Liepman AH, Olsen LJ (2001) Peroxisomal alanine:glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant J 25:487–498
• Luo S, Ishida H, Makino A, Mae T (2002) Fe2+-catalyzed sitespecific cleavage of the large subunit of ribulose 1, 5-bisphosphate carboxylase close to the active site. J Biol Chem 277:12382–12387
• Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403
• Maldonado AM, Echevarria-Zomeno S, Jean-Baptiste S, Hernandez M, Jorrin-Novo JV (2008) Evaluation of three different protocols of protein extraction for Arabidopsis thaliana leaf proteome analysis by two-dimensional electrophoresis. J Proteomics 71:461–472
• Maldonado AM, Echevarria-Zomeno S, Lindermayr C, Redondo-López I, Durner J, Jorrín-Novo J (2011) Proteomic analysis of Arabidopsis protein S-nitrosylation in response to inoculation with Pseudomonas syringae. Acta Physiol Plant. doi:10.1007/s11738-010-0688-2
• Mateo A, Muhlenbock P, Rusterucci C, Chang CC, Miszalski Z, KarpinskaB, Parker JE,MullineauxPM,Karpinski S (2004)Lesion simulating disease 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830
• Meunier B, Dumas E, Piec I, Béchet D, Hébraud M, Hocquette JF (2007) Assessment of hierarchical clustering methodologies for proteomic data mining. J Proteome Res 6:358–366
• Molina A, Mena M, Carbonero P, García-Olmedo F (1997) Differential expression of pathogen-responsive genes encoding two types of glycine-rich proteins in barley. Plant Mol Biol 33:803–810
• Naqvi SM, Park KS, Yi SY, Lee HW, Bok SH, Choi D (1998) A glycinerich RNA-binding protein gene is differentially expressed during acute hypersensitive response following Tobacco Mosaic Virus infection in tobacco. Plant Mol Biol 37:571–576
• Neuhoff V, Arold N, Taube D, EhrhardtW(1988) 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 9:255–262
• Ogawa T, Ishikawa K, Harada K, Fukusaki E, Yoshimura K, Shigeoka S (2009) Overexpression of an ADP-ribose pyrophosphatase, AtNUDX2, confers enhanced tolerance to oxidative stress in Arabidopsis plants. Plant J 57:289–301
• PawlowskiK,Twigg P,Dobritsa S,Guan C,MullinBC(1997)Anodulespecific gene family from Alnus glutinosa encodes glycine- and histidine-rich proteins expressed in the early stages of actinorhizal nodule development. Mol Plant Microbe Interact 10:656–664
• Ramagli LS, Rodríguez LV (1985) Quantitation of microgram amounts of protein in two-dimensional polyacrylamide-gel electrophoresis sample buffer electrophoresis. Electrophoresis 6:559–563
• Richman PG, Meister A (1975) The chemistry of glutathione: the work of Alton Meister. J Biol Chem 250:1422–1426
• Romero-Puertas MC, Perazzolli M, Zago ED, Delledonne M (2004) Nitric oxide signalling functions in plant–pathogen interactions. Cell Microbiol 6:795–803
• Ryser U, Schorderet M, Zhao GF, Studer D, Ruel K, Hauf G, Keller B (1997) Structural cell-wall proteins in protoxylem development: evidence for a repair process mediated by a glycine-rich protein. Plant J 12:97–111
• Scarpeci TE, Valle EM (2008) Rearrangement of carbon metabolism in Arabidopsis thaliana subjected to oxidative stress condition: an emergency survival strategy. Plant Growth Regul 54:133–142
• Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. PNAS 97:11655–11660
• Schevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing 23 of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858
• Sghaier-Hammami B, Drira N, Jorrín-Novo J (2009a) Comparative 2-DE proteomic analysis of date palm (Phoenix dactylifera L.) somatic and zygotic embryos. J Proteomics 1:161–177
• Sghaier-Hammami B, Valledor L, Drira N, Jorrin-Novo J (2009b) Proteomic analysis of the development and germination of date palm (Phoenix dactylifera L.) zygotic embryos. Proteomics 9:2543–2554
• Sghaier-Hammami B, Jorrín-Novo J, Gargouri-Bouzid R, Drira N (2011) Abscisic acid and sucrose increase the protein content in date palm somatic embryos, causing changes in 2-DE profile. Phytochemistry 71:1223–1236
• Sharov AA, Dudekula DB, Ko MS (2005) A web-based tool for PC and significance analysis of microarray data. Bioinformatics 21:2548–2549
• Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208
• Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891–904
• Taler D, Galperin M, Benjamin I, Cohen Y, Kenigsbuch D (2004) Plant ER genes that encode photorespiratory enzymes confer resistance against disease. Plant Cell 16:172–184
• Tang X, Rolee SA, Scholes JD (1996) The effect of Albugo Candida (white blister rust) on the photosynthetic and carbohydrate metabolism of leaves of Arabidopsis thaliana. Plant Cell Environ 19:967–975
• Truman W, De Torres Zabala M, Grant M (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defense responses during pathogenesis and resistance. Plant J 46:14–33
• Tsai J, DouglasMG (1996) A conserved HPD sequence of the J-domain is necessary forYDJ1 stimulation ofHsp70ATPase activity at a site distinct from substrate binding. J Biol Chem 271:9347–9354
• Valledor L, Jorrín J (2011) Back to the basics: maximizing the information obtained by quantitative two dimensional gel electrophoresis analyses by an appropriate experimental design and statistical analyses. J Proteomics 74:1–18
• Valledor L, Castillejo MA, Lenz C, Rodríguez R, Cañal MJ, Jorrín J (2008) Proteomic analysis of Pinus radiata needles: 2-DE map and protein identification by LC/MS/MS and substitutiontolerant database searching. J Proteome Res 7:2616–2631
• Van Kan JAL, Cornelissen BJC, Bol JF (1988) A virus-inducible tobáceo gene encoding a glycine-rich protein shares putative regulatory elements with the ribulose bisphosphate carboxylase small subunit gene. Mol Plant Microbe Interact 1:107–112
• Vinotha SP, Parthasarathi K, Ranganathanrefr LS (2000) Current science, enhanced phosphatase activity in earthworm casts is more of microbial origin. Sci Corresp 79:9–10
• Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040
• Wang W, Vignani R, Scali M, Cresti M (2006) A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27:2782–2786
• Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond Ser B 355:1517–1529
• Zhang G, Fenyö D, Neubert TA (2009) Evaluation of the variation in sample preparation for comparative proteomics using stable isotope labeling by amino acids in cell culture. J Proteome Res 8:1285–1292

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