Main Article Content
Due to the intensified production of reactive nitrogen species (RNS) proteins can be modified by tyrosine nitration (PTN). Examination of PTN is a hot topic of plant biology, especially because the exact outcome of this modification is still pending. Both RNS and ascorbic acid (AsA) are redox-active molecules, which directly affect the redox state of cells. The possible link between RNS-dependent PTN and AsA metabolism was studied in RNS (gsnor1-3, nia1nia2) and AsA (vtc2-3) homeostasis Arabidopsis mutants. During physiological conditions, intensified PTN was detected in all mutant lines compared to the wild-type (WT); without altering nitration pattern. Moreover, the increased PTN seemed to be associated with endogenous peroxynitrite (ONOO-) levels, but it showed no tight correlation with endogenous levels of nitric-oxide (NO) or AsA. Exogenous AsA caused intensified PTN in WT, vtc2-3 and nia1nia2. In the background of increased PTN, significant NO and ONOO- accumulation was detected, indicating exogenous AsA-induced RNS burst. Interestingly, in AsA-triggered stress-situation, changes of NO levels seem to be primarily connected to the development of PTN. Our results point out for the first time that similarly to human and animal systems exogenous AsA exerts pro-nitrant effect on plant proteome.
Asada K (1992) Ascorbate peroxidase–a hydrogen peroxide‐scavenging enzyme in plants. Physiol Plant 85(2):235-241.
Athar HUR, Khan A, Ashraf M (2009) Inducing salt tolerance in wheat by exogenously applied ascorbic acid through different modes. J Plant Nutr 32(11):1799-1817.
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exper Bot 66(19):5983-5996.
Bouayed J, Bohn T (2010) Exogenous antioxidants—doubleedged swords in cellular redox state: health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid Med Cell Longev 3(4):228-237.
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1-2):248-254.
Chaki M, de Morales PÁ, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann Bot 116(4):637-647.
Chamizo-Ampudia A, Sanz-Luque E, Llamas A, Galvan A, Fernandez E (2017) Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci 22(2):163-174.
Chao YY, Kao CH (2010) Heat shock-induced ascorbic acid accumulation in leaves increases cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 336(1-2):39-48.
Colville L, Smirnoff N (2008) Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbatedeficient Arabidopsis thaliana vtc mutants. J Exper Bot 59(14):3857-3868.
Conklin PL (2001) Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 24(4):383-394.
Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154(2):847-856.
Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49(11):1711-1722.
Corpas FJ, Luis A, Barroso JB (2007) Need of biomarkers of nitrosative stress in plants. Trends Plant Sci 12(10):436-438.
Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57(3):471-478.
Denicola A, Souza JM, Radi R (1998) Diffusion of peroxynitrite across erythrocyte membranes. Proceedings of the National Academy of Sciences 95(7):3566-3571.
Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. PNAS 102(22):8054-8059.
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133(1):21-25.
Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H (2004) Biological significance of nitric oxide-mediated protein modifications. Am J Physiol Lung Cell Mol Physiol 287(2):262-268.
Greenacre SA, Ischiropoulos H (2001) Tyrosine nitration: localisation, quantification, consequences for protein function and signal transduction. Free Rad Res 34(6):541-581.
Kashiba-Iwatsuki M, Yamaguchi M, Inoue M (1996) Role of ascorbic acid in the metabolism of S‐nitroso‐glutathione. FEBS Letters 389(2):149-152.
Kolbert Zs, Feigl G, Bordé Á, Molnár Á, Erdei L (2017) Protein tyrosine nitration in plants: Present knowledge, computational prediction and future perspectives. Plant Physiol Biochem 113:56-63.
Kolbert Zs, Pető A, Lehotai N, Feigl G, Ördög A, Erdei L (2012) In vivo and in vitro studies on fluorophorespecificity. Acta Biol Szeged 56(1):37-41.
Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of paraquat. Biochem J 210(3):899-903.
Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20(3):786-802.
Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137(3):921-930.
Mata-Pérez C, Begara-Morales JC, Chaki M, Sánchez-Calvo B, Valderrama R, Padilla MN, Corpas FJ, Barroso JB (2016) Protein tyrosine nitration during development Pro-nitrant properties of exogenous ascorbate and abiotic stress response in plants. Frontiers Plant Sci 7:1699.
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473-497.
Padh H (1990) Cellular functions of ascorbic acid. Biochem Cell Biol 68(10):1166-1173.
Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, Darley-Usmar VM (1999) Biological aspects of reactive nitrogen species. BBA-Bioenergetics 1411(2):385-400.
Pető A, Lehotai N, Lozano-Juste J, León J, Tari I, Erdei L, Kolbert Zs (2011) Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Ann Bot 108(3):449-457.
Qian HF, Peng XF, Han X, Ren J, Zhan KY, Zhu M (2014) The stress factor, exogenous ascorbic acid, affects plant growth and the antioxidant system in Arabidopsis thaliana. Russian J Plant Physiol 61(4):467-475.
Radi R (2004) Nitric oxide, oxidants, and protein tyrosine nitration. PNAS 101(12):4003-4008.
Radi R (2012) Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Accounts Chem Res 46(2):550-559.
Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC (2007) S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143(3):1282-1292.
Sarkar TS, Biswas P, Ghosh SK, Ghosh S (2014) Nitric oxide production by necrotrophic pathogen Macrophomina phaseolina and the host plant in charcoal rot disease of jute: Complexity of the interplay between necrotroph–host plant interactions. PloS One 9(9):e107348.
Seligman K, Saviani EE, Oliveira HC, Pinto-Maglio CAF, Salgado I (2008) Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants. Plant Cell Physiol 49(7):1112-1121.
Souza JM, Peluffo G, Radi R (2008) Protein tyrosine nitration—functional alteration or just a biomarker? Free Rad Biol Med 45(4):357-366.
Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative‐based signaling and associated post‐translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72(4):585-599.
Tyburski J, Dunajska-Ordak K, Skorupa M, Tretyn A (2012) Role of ascorbate in the regulation of the Arabidopsis thaliana root growth by phosphate availability. J Bot 2012:580342.
Wang Y, Loake GJ, Chu C (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Frontiers Plant Sci 4:314.
Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239(1-2):289-297.
Yeo WS, Kim YJ, Kabir MH, Kang JW, Kim K (2015) Mass spectrometric analysis of protein tyrosine nitration in aging and neurodegenerative diseases. Mass Spectrom Rev 34(2):166-183.