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

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Abstract

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.

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Abbreviations

APX:

Ascorbate peroxidase

DHAR2:

Dehydroascorbate reductase

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

GSNO:

S-nitrosoglutathione

GST:

Glutathion-S-transferase

HR:

Hypersensitive response

MDH:

Malate dehydrogenase

MMTS:

Methyl methanethiosulfonate

NO:

Nitric oxide

PAMPs:

Pathogen-associated molecular patterns

Prx:

Peroxiredoxin

PSII:

Photosystem II

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

SA:

Salycilyc acid

SAM:

S-adenosyl methionine

SAMS:

S-adenosyl methionine synthetase

References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Alban D, Job D, Douce R (2000) Biotin metabolism in plants. Ann Rev Plant Biochem Plant Mol Biol 51:17–47

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bednarek P, Osbourn A (2009) Plant-microbe interactions: chemical diversity in plant defense. Science 324:746–748

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Coaker G, Falick A, Staskawicz B (2005) Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548–550

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:1–10

    Article  Google Scholar 

  • Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244

    Article  PubMed  CAS  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374

    Article  PubMed  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Foster MW, Stamler JS (2004) New insights into protein Snitrosylation. Mitochondria as a model system. J Biol Chem 279:25891–25897

    Article  PubMed  CAS  Google Scholar 

  • Foster MW, Liu L, Zeng M, Hess DT, Stamler JS (2009) A genetic analysis of nitrosative stress. Biochemistry 48:792–799

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hao G, Xie L, Gross SS (2004) Argininosuccinate synthetase is reversibly inactivated by S-nitrosylation in vitro and in vivo. JBC 279:36192–36200

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annu Rev Phytopathol 47:153–176

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Kim J, Kim HY (2006) Molecular characterization of a bHLH transcription factor involved in Arabidopsis abscisic acid-mediated response. Biochim Biophys Acta 1759:191–194

    PubMed  CAS  Google Scholar 

  • Kobayashi Y, Kobayashi I (2009) Depolymerization of the actin cytoskeleton induces defense responses in tobacco plants. J Gen Plant Pathol 73:360–364

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Markham GD, Pajares MA (2009) Structure-function relationships in methionine adenosyltransferases. Cell Mol Life Sci. 66, 636-648

    Google Scholar 

  • Martínez-Ruiz A, Lamas S (2004) Detection and proteomic identification of S-nitrosylated proteins in endothelial cells. Arch. Biochem. Biophys 423:192–199

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Stamler JS, Lamas S, Fang FC (2001) Nitrosylation the prototypic redox-based signaling mechanism. Cell 106:675–683

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Annals of Botany 105:1–6

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Yamasaki H (2002) Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett 512:145–148

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhao S, Qi X (2008) Signaling in plant disease resistance and symbiosis. J Integr Plant Biol 50:799–807

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was carried out with financial support from the Spanish “Ministerio de Educación y Ciencia”, Project BIO-2006-14790. The MS analysis was conducted in the Proteomics Unit (SCAI) at Córdoba University. SEZ is supported by a grant from the the Spanish “Ministerio de Educación y Ciencia”.

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Correspondence to Ana M. Maldonado-Alconada.

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Communicated by M. Hajduch.

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Maldonado-Alconada, A.M., Echevarría-Zomeño, S., Lindermayr, C. et al. Proteomic analysis of Arabidopsis protein S-nitrosylation in response to inoculation with Pseudomonas syringae . Acta Physiol Plant 33, 1493–1514 (2011). https://doi.org/10.1007/s11738-010-0688-2

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