Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i>
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 NO<sub>2</sub> group to a tyrosine residue, can modulate reduced nicotinamide...
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MDPI AG
2019-10-01
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| Series: | Antioxidants |
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| Online Access: | https://www.mdpi.com/2076-3921/8/10/448 |
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| author | Juan C. Begara-Morales Beatriz Sánchez-Calvo María V. Gómez-Rodríguez Mounira Chaki Raquel Valderrama Capilla Mata-Pérez Javier López-Jaramillo Francisco J. Corpas Juan B. Barroso |
| author_facet | Juan C. Begara-Morales Beatriz Sánchez-Calvo María V. Gómez-Rodríguez Mounira Chaki Raquel Valderrama Capilla Mata-Pérez Javier López-Jaramillo Francisco J. Corpas Juan B. Barroso |
| author_sort | Juan C. Begara-Morales |
| collection | DOAJ |
| description | 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 NO<sub>2</sub> 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 <i>Arabidopsis thaliana</i> 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 <i>Arabidopsis</i> 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. |
| first_indexed | 2024-03-12T05:42:48Z |
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| institution | Directory Open Access Journal |
| issn | 2076-3921 |
| language | English |
| last_indexed | 2024-03-12T05:42:48Z |
| publishDate | 2019-10-01 |
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| series | Antioxidants |
| spelling | doaj.art-b65a62cfb7d24629a31dd298a0cb85f82023-09-03T05:54:03ZengMDPI AGAntioxidants2076-39212019-10-0181044810.3390/antiox8100448antiox8100448Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i>Juan C. Begara-Morales0Beatriz Sánchez-Calvo1María V. Gómez-Rodríguez2Mounira Chaki3Raquel Valderrama4Capilla Mata-Pérez5Javier López-Jaramillo6Francisco J. Corpas7Juan B. Barroso8Group of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, Faculty of Experimental Sciences, University of Jaén, Campus “Las Lagunillas”, s/n, E-23071 Jaén, SpainGroup of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, Faculty of Experimental Sciences, University of Jaén, Campus “Las Lagunillas”, s/n, E-23071 Jaén, SpainGroup of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, Faculty of Experimental Sciences, University of Jaén, Campus “Las Lagunillas”, s/n, E-23071 Jaén, SpainGroup of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, Faculty of Experimental Sciences, University of Jaén, Campus “Las Lagunillas”, s/n, E-23071 Jaén, SpainGroup of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, Faculty of Experimental Sciences, University of Jaén, Campus “Las Lagunillas”, s/n, E-23071 Jaén, SpainGroup of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, Faculty of Experimental Sciences, University of Jaén, Campus “Las Lagunillas”, s/n, E-23071 Jaén, SpainInstitute of Biotechnology, Department of Organic Chemistry, Faculty of Sciences, University of Granada, E-18071 Granada, SpainGroup of Antioxidants, Free Radicals, and Nitric Oxide in Biotechnology, Food and Agriculture, Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental del Zaidín, CSIC, C/Profesor Albareda 1, E-18080 Granada, SpainGroup of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, Faculty of Experimental Sciences, University of Jaén, Campus “Las Lagunillas”, s/n, E-23071 Jaén, SpainLow 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 NO<sub>2</sub> 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 <i>Arabidopsis thaliana</i> 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 <i>Arabidopsis</i> 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.https://www.mdpi.com/2076-3921/8/10/448nadp malic enzymelow temperaturenitric oxidetyrosine nitrationperoxynitritereactive oxygen speciesreactive nitrogen speciesnitro-oxidative stress |
| spellingShingle | Juan C. Begara-Morales Beatriz Sánchez-Calvo María V. Gómez-Rodríguez Mounira Chaki Raquel Valderrama Capilla Mata-Pérez Javier López-Jaramillo Francisco J. Corpas Juan B. Barroso Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i> Antioxidants nadp malic enzyme low temperature nitric oxide tyrosine nitration peroxynitrite reactive oxygen species reactive nitrogen species nitro-oxidative stress |
| title | Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i> |
| title_full | Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i> |
| title_fullStr | Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i> |
| title_full_unstemmed | Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i> |
| title_short | Short-Term Low Temperature Induces Nitro-Oxidative Stress that Deregulates the NADP-Malic Enzyme Function by Tyrosine Nitration in <i>Arabidopsis thaliana</i> |
| title_sort | short term low temperature induces nitro oxidative stress that deregulates the nadp malic enzyme function by tyrosine nitration in i arabidopsis thaliana i |
| topic | nadp malic enzyme low temperature nitric oxide tyrosine nitration peroxynitrite reactive oxygen species reactive nitrogen species nitro-oxidative stress |
| url | https://www.mdpi.com/2076-3921/8/10/448 |
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