Proteomic analysis of Arabidopsis protein S-nitrosylation in response to inoculation with Pseudomonas syringae

• Autorzy: Maldonado-Alconada A.M. , Echevarria-Zomeno S. , Lindermayr C. , Redondo-Lopez I. , Durner J. , Jorrin-Novo J. V.
• Języki publikacji: EN

Abstrakty

EN

Nitric oxide (NO) is a key signaling molecule in plants, being its biological effects mainly mediated through S-nitrosylation of cysteine thiols. Using the biotin switch method combined with mass spectrometry analysis we have identified 127 targets of S-nitrosylation in Arabidopsis cell suspension cultures and leaves challenged with virulent and avirulent isolates of Pseudomonas syringae pv. tomato. The NO targets are proteins associated with carbon, nitrogen, and sulpfur metabolism, photosynthesis, the cytoskeleton, stress-, pathogen- and redox-related and signaling proteins. Some proteins were previously identified in plants and mammals, while others (63%) represent novel targets of S-nitrosylation. Our data suggest that NO might be orchestrating the whole plant physiology, presumably through covalent modification of proteins.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2011
• Tom: 33
• Numer: 4
• Opis fizyczny: p.1493-1514,fig.,ref.

Twórcy

autor

Maldonado-Alconada A.M.

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

autor

Echevarria-Zomeno S.

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

autor

Lindermayr C.

• Institute of Biochemical Plant Pathology, Helmholtz Zentrum Munchen-German Research Center for Environmental Health, 85764, Neuherberg, Germany

autor

Redondo-Lopez I.

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

autor

Durner J.

• Institute of Biochemical Plant Pathology, Helmholtz Zentrum München-German Research Center for Environmental Health, 85764, Neuherberg, Germany

autor

Jorrin-Novo J. V.

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

Bibliografia

• Abat JK, Mattoo AK, Deswal R (2008) S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata-ribulose-1,5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS J 275:2862–2872
• Alban D, Job D, Douce R (2000) Biotin metabolism in plants. Ann Rev Plant Biochem Plant Mol Biol 51:17–47
• Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077–2080
• Bartberger MD, Mannion JD, Powell SC, Stamler JS, Houk KN, Toone EJ (2001) S-N dissociation energies of S-nitrosothiols: on the origins of nitrosothiol decomposition rates. J Am Chem Soc 123:8868–8869
• Bednarek P, Osbourn A (2009) Plant-microbe interactions: chemical diversity in plant defense. Science 324:746–748
• Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inzé D, Delledonne M, Van Breusegem F (2007) Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem 282:1352–1358
• Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39
• Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye biding. Anal Biochem 72:248–254
• Caporn SJM, Hand DW, Mansfield TA, Wellburn AR (1994) Canopy photosynthesis of CO₂-enriched lettuce (Lactuca sativa L.).
• Response to short-term changes in CO₂, temperature and oxides of nitrogen. New Phytol 126:45–52
• Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodríguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunfl ower–mildew interaction. Plant Cell Physiol 50:265–279
• Chandra-Shekara AC, Venugopal SC, Barman SR, Kachroo A, Kachroo P (2007) Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis. Proc Natl Acad Sci USA 104:7277–7282
• Coaker G, Falick A, Staskawicz B (2005) Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548–550
• Curto M, Camafeita E, Lopez JA, Maldonado AM, Rubiales D, Jorrín JV. (2006) A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi) proteomics 6(Suppl 1):S163–S714
• Dangl JL, McDowell JM (2006) Two modes of pathogen recognition by plants. Proc Natl Acad Sci USA 103:8575–8576
• Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281
• Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588
• Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459
• Dietz K-J, Jacob S, Oelze M-L, Laxa M, Tognetti V, Nunes de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709
• Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:1–10
• Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244
• Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374
• Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
• Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F, De Los Santos B, Romero F, Pliego-Alfaro F, Muñoz-Blanco J, Caballero JL (2009) Evidence for a positive regulatory role of strawberry (Fragaria × ananassa) FaWRKY1 and Arabidopsis at WRKY75 proteins in resistance. J Exp Bot 60:3043–3065
• Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371
• Feechan A, Kwon E, Yun B-W, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. PNAS 102:8054–8059
• Foster MW, Stamler JS (2004) New insights into protein Snitrosylation. Mitochondria as a model system. J Biol Chem 279:25891–25897
• Foster MW, Liu L, Zeng M, Hess DT, Stamler JS (2009) A genetic analysis of nitrosative stress. Biochemistry 48:792–799
• Gomez-Ariza J, Campo S, Rufat M, Estopa M, Messequer J, San Sequndo B, Coca M (2007) Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms proteins in rice plant. Mol Plant Microbe Interact 20:832–842
• Greco TM, Hodara R, Parastatidis I, Heijnen HF, Dennehy MK, Liebler DC, Ischiropoulos H (2006) Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc Natl Acad Sci USA 103:7420–7425
• Hao G, Xie L, Gross SS (2004) Argininosuccinate synthetase is reversibly inactivated by S-nitrosylation in vitro and in vivo. JBC 279:36192–36200
• Hao G, Derakhshan B, Shi L, Campagne F, Gross SS (2006) SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. Proc Natl Acad Sci USA 103:1012–1017
• Hara MR, Agrawal N, Kim SF, Cascio MB, Fujimuro M, Ozeki Y, Takahashi M, Cheah JH, Tankou SK, Hester LD, Ferris CD, Hayward SD, Snyder SH, Sawa A (2005) Snitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7:665–674
• Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166
• Huang B, Chen C (2006) An ascorbate-dependent artifact that interferes with the interpretation of the biotin switch assay. Free Radic Biol Med 4:562–567
• Huang X, von Rad U, Durner J (2002) Nitric oxide induces the nitric oxide tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923
• Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3:193–197
• 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
• Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annu Rev Phytopathol 47:153–176
• Kasprowicz A, Szuba A, Volkmann D, Baluska F, Wojtaszek P (2009) Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices. J Exp Bot 60:1605–1617
• Kiddle G, Pastori GM, Bernard S, Pignocchi C, Antoniw J, Verrier PJ, Foyer CH (2003) Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid Redox Signal 5:23–32
• Kim J, Kim HY (2006) Molecular characterization of a bHLH transcription factor involved in Arabidopsis abscisic acidmediated response. Biochim Biophys Acta 1759:191–194
• Kobayashi Y, Kobayashi I (2009) Depolymerization of the actin cytoskeleton induces defense responses in tobacco plants. J Gen Plant Pathol 73:360–364
• Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
• Lai Z, Vinod K, Zheng Z, Fan B, Chen Z. (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. 1. BMC Plant Biol 8:68
• Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of s-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930
• Lindermayr C, Saalbach G, Bahnweg G, Durner J (2006) Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J Biol Chem 281:4285–4291
• 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
• Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410
• Marcus Y, Altman-Gueta H, Finkler A, Gurevitz M (2003) Dual role of cysteine 172 in redox regulation of ribulose 1, 5- bisphosphate carboxylase/oxygenase activity and degradation. J Bacteriol 185:1509–1517
• Markham GD, Pajares MA (2009) Structure-function relationships in methionine adenosyltransferases. Cell Mol Life Sci. 66, 636-648
• Martínez-Ruiz A, Lamas S (2004) Detection and proteomic identification of S-nitrosylated proteins in endothelial cells. Arch. Biochem. Biophys 423:192–199
• Martínez-Ruiz A, Villanueva L, González de Orduña C, López-Ferrer D, Higueras MA, Tarín C, Rodríguez-Crespo I, Vázquez J, Lamas S (2005) S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities Proc Natl Acad Sci USA 102:8525–8530
• Padgett CM, Whorton AR (1995) S-nitrosoglutathione reversibly inhibits GAPDH by S-nitrosylation. Am J Physiol 269:C739–C749
• Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lindermayr C (2008) Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59:177–186
• Palmieri MC, Lindermayr C, Bauwe H, Steinhauser C, Durner J (2010) Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol 152:1514–1528
• Parker D, Beckmann M, Zubair H, Enot DP, Caracuel-Rios Z, Overy DP, Snowdon S, Talbot NJ, Draper J (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant Journal 59:723–737
• Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Lamb C, Delledonne M (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16:2785–2794
• Pérez-Bueno ML, Rahoutei J, Sajnani C, García-Luque I, Barón M (2004) Proteomic analysis of the oxygen-evolving complex of photosystem II under biotec stress: Studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4:418–425
• Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric Oxide-Mediated Transcriptional Changes in Arabidopsis thaliana. Mol. Plant. Microbe Interact 16:1094–1105
• Reuber TL, Ausubel FM (1996) Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 8:241–249
• Rhee KY, Erdjument-Bromage H, Tempst P, Nathan CF (2005) S-nitrosoproteome of Mycobacterium tuberculosis: enzymes of intermediary metabolism and antioxidant defense. Proc Natl Acad Sci USA 102:467–472
• Rocha PS, Sheikh M, Melchiorre R, Fagard M, Boutet S, Loach R, Moffatt B, Wagner C, Vaucheret H, Furner I (2005) The Arabidopsis HOMOLOGY-DEPENDENT GENE SILENCING1 gene codes for an S-adenosyl-L-homocysteine hydrolase required for DNA methylation-dependent gene silencing. Plant Cell 17:404–417
• Rodríguez-Pascual F, Redondo-Horcajo M, Magán-Marchal N, Lagares D, Martínez-Ruiz A, Kleinert H, Lamas S (2008) Glyceraldehyde-3-phosphate dehydrogenase regulates endothelin- 1 expression by a novel, redox-sensitive mechanism involving mRNA stability. Mol Cell Biol 28:7139–7155
• Romero-Puertas MC, Laxa M, Matte A, Zaninotto F, Finkemeier I, Jones AM, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130
• Romero-Puertas MC, Campostrini N, Matte A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469
• Sakamoto A, Tsukamoto S, Yamamoto H, Ueda-Hashimoto M, Takahashi M, Suzuki H, Morikawa H (2003) Functional complementation in yeast reveals a protective role of chloroplast 2-Cys peroxiredoxin against reactive nitrogen species. Plant J 33:841–851
• Schaarschmidt S, Kopka J, Ludwig-Muller J, Hause B (2007) Regulation of arbuscular mycorrhization by apoplastic invertases: enhanced invertase activity in the leaf apoplast affects the symbiotic interaction. Plant J 51:390–405
• Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenz H (2007) Inhibition of AtMYB2 DNA-binding by nitric oxide involvescysteine S-nitrosylation. Biochem. Biophys Res. Commun 361:1048–1053
• Sokolovski S, Blatt MR (2004) Nitric Oxide Block of Outward-Rectifying K1 Channels Indicates Direct Control by Protein Nitrosylation in Guard Cells. Plant Physiol 136:4275–4284
• Stamler JS, Lamas S, Fang FC (2001) Nitrosylation the prototypic redox-based signaling mechanism. Cell 106:675–683
• Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956
• Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Annals of Botany 105:1–6
• Takahashi S, Yamasaki H (2002) Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett 512:145–148
• Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. The Plant Journal 60:795–804
• Trujillo M, Ichimura K, Casais C, Shirasu K (2008) Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr Biol 18:1396–1401
• 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
• Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354
• Wang YQ, Feechan A, Yun BW, Shafiei R, Hofmann A, Taylor P, Xue P, Yang FQ, Xie ZS, Pallas JA, Chu CC, Loake GJ (2009) S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J Biol Chem 284:2131–2137
• Yoda H, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H (2009) Polyamines as a common source of hydrogen peroxide in host- and nonhost hypersensitive response during pathogen infection. Plant Mol Biol 70:103–112
• Zhao S, Qi X (2008) Signaling in plant disease resistance and symbiosis. J Integr Plant Biol 50:799–807

Uwagi

PL

Rekord w opracowaniu