Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana
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...
| Autores: | , , , , , , , , |
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| Formato: | artículo |
| Estado: | Versión publicada |
| Fecha de publicación: | 2019 |
| País: | España |
| Recursos: | Consejo Superior de Investigaciones Científicas (CSIC) |
| Repositorio: | DIGITAL.CSIC. Repositorio Institucional del CSIC |
| OAI Identifier: | oai:digital.csic.es:10261/193483 |
| Acesso em linha: | http://hdl.handle.net/10261/193483 |
| Access Level: | acceso abierto |
| Palavra-chave: | NADP malic enzyme Low temperature Nitric oxide tyrosine nitration Peroxynitrite Reactive oxygen species Reactive nitrogen species Nitro-oxidative stress |
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Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thalianaBegara Morales, Juan CarlosSánchez-Calvo, BeatrizGómez-Rodríguez, María V.Chaki, MouniraValderrama, RaquelMata-Pérez, CapillaLópez-Jaramillo, JavierCorpas, Francisco J.Barroso-Albarracín, Juan BautistaNADP malic enzymeLow temperatureNitric oxidetyrosine nitrationPeroxynitriteReactive oxygen speciesReactive nitrogen speciesNitro-oxidative stressLow 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.Technical and human support provided by CICT of Universidad de Jaén (UJA, MINECO, Junta de Andalucía, and FEDER) is gratefully acknowledged.Peer reviewedMultidisciplinary Digital Publishing InstituteUniversidad de JaénMinisterio de Economía y Competitividad (España)Junta de AndalucíaEuropean CommissionConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2019201920192019info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/193483reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttps://www.mdpi.com/2076-3921/8/10/448SíSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1934832026-05-22T06:33:51Z |
| dc.title.none.fl_str_mv |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana |
| title |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana |
| spellingShingle |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana Begara Morales, Juan Carlos NADP malic enzyme Low temperature Nitric oxide tyrosine nitration Peroxynitrite Reactive oxygen species Reactive nitrogen species Nitro-oxidative stress |
| title_short |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana |
| title_full |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana |
| title_fullStr |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana |
| title_full_unstemmed |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana |
| title_sort |
Short-term low temperature induces nitro-oxidative stress that deregulates the NADP-Malic enzyme function by tyrosine nitration in arabidopsis thaliana |
| dc.creator.none.fl_str_mv |
Begara Morales, Juan Carlos Sánchez-Calvo, Beatriz Gómez-Rodríguez, María V. Chaki, Mounira Valderrama, Raquel Mata-Pérez, Capilla López-Jaramillo, Javier Corpas, Francisco J. Barroso-Albarracín, Juan Bautista |
| author |
Begara Morales, Juan Carlos |
| author_facet |
Begara Morales, Juan Carlos Sánchez-Calvo, Beatriz Gómez-Rodríguez, María V. Chaki, Mounira Valderrama, Raquel Mata-Pérez, Capilla López-Jaramillo, Javier Corpas, Francisco J. Barroso-Albarracín, Juan Bautista |
| author_role |
author |
| author2 |
Sánchez-Calvo, Beatriz Gómez-Rodríguez, María V. Chaki, Mounira Valderrama, Raquel Mata-Pérez, Capilla López-Jaramillo, Javier Corpas, Francisco J. Barroso-Albarracín, Juan Bautista |
| author2_role |
author author author author author author author author |
| dc.contributor.none.fl_str_mv |
Universidad de Jaén Ministerio de Economía y Competitividad (España) Junta de Andalucía European Commission Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72] Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72] |
| dc.subject.none.fl_str_mv |
NADP malic enzyme Low temperature Nitric oxide tyrosine nitration Peroxynitrite Reactive oxygen species Reactive nitrogen species Nitro-oxidative stress |
| topic |
NADP malic enzyme Low temperature Nitric oxide tyrosine nitration Peroxynitrite Reactive oxygen species Reactive nitrogen species Nitro-oxidative stress |
| 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 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. |
| publishDate |
2019 |
| dc.date.none.fl_str_mv |
2019 2019 2019 2019 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article http://purl.org/coar/resource_type/c_6501 Publisher's version info:eu-repo/semantics/publishedVersion |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.none.fl_str_mv |
http://hdl.handle.net/10261/193483 |
| url |
http://hdl.handle.net/10261/193483 |
| dc.language.none.fl_str_mv |
Inglés |
| language_invalid_str_mv |
Inglés |
| dc.relation.none.fl_str_mv |
https://www.mdpi.com/2076-3921/8/10/448 Sí Sí |
| dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess |
| eu_rights_str_mv |
openAccess |
| dc.publisher.none.fl_str_mv |
Multidisciplinary Digital Publishing Institute |
| publisher.none.fl_str_mv |
Multidisciplinary Digital Publishing Institute |
| dc.source.none.fl_str_mv |
reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC) |
| instname_str |
Consejo Superior de Investigaciones Científicas (CSIC) |
| reponame_str |
DIGITAL.CSIC. Repositorio Institucional del CSIC |
| collection |
DIGITAL.CSIC. Repositorio Institucional del CSIC |
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| repository.mail.fl_str_mv |
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1869405002550738944 |
| score |
15.198674 |