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...

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Autores: 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
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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spelling 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


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
repository.name.fl_str_mv
repository.mail.fl_str_mv
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