Arsenic-induced stress activates sulfur metabolism in different organs of garlic (Allium sativum L.) plants accompanied by a general decline of the NADPH-generating systems in roots

Ruíz-Torres, Carmelo; Feriche-Linares, Rafael; Rodríguez-Ruiz, Marta; Palma, José M.; Corpas, Francisco J.

doi:10.1016/j.jplph.2016.12.010

Cited by 54 publications

(19 citation statements)

References 63 publications

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“…It is considered a redox guardian of these organelles due to its potentially important role in signaling processes in peroxisomes and other intracellular compartments [3]. Changes in catalase activity have been found to be a major monitoring index of plant responses under abiotic or biotic conditions [2,6,45,57,58]. A more recent study of expression profiling of both A. thaliana and Oryza sativa using transcriptomic and proteomic techniques, which erroneously reported that the catalase protein was also localized in the cytosol, found that catalase plays specific roles in development and stress responses [59].…”

Section: Discussionmentioning

confidence: 99%

Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species

et al. 2019

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During the ripening of sweet pepper (Capsicum annuum L.) fruits, in a genetically controlled scenario, enormous metabolic changes occur that affect the physiology of most cell compartments. Peroxisomal catalase gene expression decreases after pepper fruit ripening, while the enzyme is also susceptible to undergo post-translational modifications (nitration, S-nitrosation, and oxidation) promoted by reactive oxygen and nitrogen species (ROS/RNS). Unlike most plant catalases, the pepper fruit enzyme acts as a homodimer, with an atypical native molecular mass of 125 to 135 kDa and an isoelectric point of 7.4, which is higher than that of most plant catalases. These data suggest that ROS/RNS could be essential to modulate the role of catalase in maintaining basic cellular peroxisomal functions during pepper fruit ripening when nitro-oxidative stress occurs. Using catalase from bovine liver as a model and biotin-switch labeling, in-gel trypsin digestion, and nanoliquid chromatography coupled with mass spectrometry, it was found that Cys377 from the bovine enzyme could potentially undergo S-nitrosation. To our knowledge, this is the first report of a cysteine residue from catalase that can be post-translationally modified by S-nitrosation, which makes it especially important to find the target points where the enzyme can be modulated under either physiological or adverse conditions.

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Section: Discussionmentioning

confidence: 99%

Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species

et al. 2019

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“…Different NADP-dehydrogenases have been shown to be modulated by diverse types of abiotic stresses; e.g., heavy metal [17,111,112], ozone [113], salinity [18,23,114,115], drought [116], and wounding [117]. In pea plants left under natural senescence conditions in which ROS and RNS increased, we also recently identified Tyr392 to be a target of tyrosine nitration that inhibits cytosolic NADP-ICDH [42].…”

Section: Discussionmentioning

confidence: 99%

Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in Arabidopsis thaliana

et al. 2019

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Low temperature (LT) negatively affects plant growth and development via the alteration of the metabolism of reactive oxygen and nitrogen species (ROS and RNS). Among RNS, tyrosine nitration, the addition of an NO2 group to a tyrosine residue, can modulate reduced nicotinamide-dinucleotide phosphate (NADPH)-generating systems and, therefore, can alter the levels of NADPH, a key cofactor in cellular redox homeostasis. NADPH also acts as an indispensable electron donor within a wide range of enzymatic reactions, biosynthetic pathways, and detoxification processes, which could affect plant viability. To extend our knowledge about the regulation of this key cofactor by this nitric oxide (NO)-related post-translational modification, we analyzed the effect of tyrosine nitration on another NADPH-generating enzyme, the NADP-malic enzyme (NADP-ME), under LT stress. In Arabidopsis thaliana seedlings exposed to short-term LT (4 °C for 48 h), a 50% growth reduction accompanied by an increase in the content of superoxide, nitric oxide, and peroxynitrite, in addition to diminished cytosolic NADP-ME activity, were found. In vitro assays confirmed that peroxynitrite inhibits cytosolic NADP-ME2 activity due to tyrosine nitration. The mass spectrometric analysis of nitrated NADP-ME2 enabled us to determine that Tyr-73 was exclusively nitrated to 3-nitrotyrosine by peroxynitrite. The in silico analysis of the Arabidopsis NADP-ME2 protein sequence suggests that Tyr73 nitration could disrupt the interactions between the specific amino acids responsible for protein structure stability. In conclusion, the present data show that short-term LT stress affects the metabolism of ROS and RNS, which appears to negatively modulate the activity of cytosolic NADP-ME through the tyrosine nitration process.

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“…Nevertheless, the differential response of the principal NADPH-generating enzymes in pepper, which depend on the organs, stage of development, plant species and stress conditions analyzed, is unsurprising (Valderrama et al 2006, Mateos et al 2009, Mateos et al 2013, Manai et al 2014, Bouthour et al 2015, Kharbech et al 2017, Hýsková et al 2017, Ruíz-Torres et al 2017, Houmani et al 2018. Analysis of these enzymes in the principal pepper seedling organs (roots, stems and leaves) during their early stage of development showed that NADP-ICDH and NADP-ME activity was highest in roots (Airaki et al 2015).…”

Section: Nadph Supply Is Mainly Provided By 6pgdh and Nadp-me Activitmentioning

confidence: 99%

“…However, other molecules, including glutathione (GSH), with its antioxidant properties, S-nitrosoglutahtione (GSNO), as well as the nitric oxide (NO) reservoir, have important physiological functions (Hogg 2002, Broniowska et al 2013, Corpas et al 2013a, 2013b. Other secondary sulfur compounds, including polysulfides (Münchberg et al 2007), glucosinolates (Hasanuzzaman et al 2017) and phytochelatins, which play important physiological roles, are involved in mechanisms of response to stress (Gupta et al 2013, Ruíz-Torres et al 2017. Hydrogen sulfide (H 2 S), which is generated in the Cys metabolism, is now recognized as an important signaling molecule capable of regulating proteins through a posttranslational modification called persulfidation (Filipovic andJovanovic 2017, Aroca et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Muñoz‐Vargas

González‐Gordo

Palma

et al. 2019

Physiologia Plantarum

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NADPH is an essential cofactor in many physiological processes. Fruit ripening is caused by multiple biochemical pathways in which, reactive oxygen and nitrogen species (ROS/RNS) metabolism is involved. Previous studies have demonstrated the differential modulation of nitric oxide (NO) and hydrogen sulfide (H2S) content during sweet pepper (Capsicum annuum L.) fruit ripening, both of which regulate NADP‐isocitrate dehydrogenase activity. To gain a deeper understanding of the potential functions of other NADPH‐generating components, we analyzed glucose‐6‐phosphate dehydrogenase (G6PDH) and 6‐phosphogluconate dehydrogenase (6PGDH), which are involved in the oxidative phase of the pentose phosphate pathway (OxPPP) and NADP‐malic enzyme (NADP‐ME). During fruit ripening, G6PDH activity diminished by 38%, while 6PGDH and NADP‐ME activity increased 1.5‐ and 2.6‐fold, respectively. To better understand the potential regulation of these NADP‐dehydrogenases by H2S, we obtained a 50–75% ammonium‐sulfate‐enriched protein fraction containing these proteins. With the aid of in vitro assays, in the presence of H2S, we observed that, while NADP‐ME activity was inhibited by up to 29–32% using 2 and 5 mM Na2S as H2S donor, G6PDH and 6PGDH activities were unaffected. On the other hand, NO donors, S‐nitrosocyteine (CysNO) and DETA NONOate also inhibited NADP‐ME activity by 35%. These findings suggest that both NADP‐ME and 6PGDH play an important role in maintaining the supply of NADPH during pepper fruit ripening and that H2S and NO partially modulate the NADPH‐generating system.

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Arsenic-induced stress activates sulfur metabolism in different organs of garlic (Allium sativum L.) plants accompanied by a general decline of the NADPH-generating systems in roots

Cited by 54 publications

References 63 publications

Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species

Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species

Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in Arabidopsis thaliana

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

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Arsenic-induced stress activates sulfur metabolism in different organs of garlic (Allium sativum L.) plants accompanied by a general decline of the NADPH-generating systems in roots

Cited by 54 publications

References 63 publications

Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species

Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species

Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in Arabidopsis thaliana

Inhibition of NADP‐malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits

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Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits