Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment

Superoxide radical (O) is involved in numerous physiological and stress processes in higher plants. Fruit ripening encompasses degradative and biosynthetic pathways including reactive oxygen and nitrogen species. With the use of sweet pepper (Capsicum annuum L.) fruits at different ripening stages a...

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Authors: González-Gordo, Salvador, Rodríguez-Ruiz, Marta, Palma Martínez, José Manuel, Corpas, Francisco J.
Format: article
Status:Published version
Publication Date:2020
Country:España
Institution:Consejo Superior de Investigaciones Científicas (CSIC)
Repository:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/218088
Online Access:http://hdl.handle.net/10261/218088
Access Level:Open access
Keyword:NADPH oxidase
Nitric oxide
Nitration
Pepper fruit
Respiratory burst oxidase homolog
S-nitrosation
Superoxide dismutase
Ripening
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spelling Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environmentGonzález-Gordo, SalvadorRodríguez-Ruiz, MartaPalma Martínez, José ManuelCorpas, Francisco J.NADPH oxidaseNitric oxideNitrationPepper fruitRespiratory burst oxidase homologS-nitrosationSuperoxide dismutaseRipeningSuperoxide radical (O) is involved in numerous physiological and stress processes in higher plants. Fruit ripening encompasses degradative and biosynthetic pathways including reactive oxygen and nitrogen species. With the use of sweet pepper (Capsicum annuum L.) fruits at different ripening stages and under a nitric oxide (NO)-enriched environment, the metabolism of O was evaluated at biochemical and molecular levels considering the O generation by a NADPH oxidase system and its dismutation by superoxide dismutase (SOD). At the biochemical level, seven O-generating NADPH-dependent oxidase isozymes [also called respiratory burst oxidase homologs (RBOHs) I–VII], with different electrophoretic mobility and abundance, were detected considering all ripening stages from green to red fruits and NO environment. Globally, this system was gradually increased from green to red stage with a maximum of approximately 2.4-fold increase in red fruit compared with green fruit. Significantly, breaking-point (BP) fruits with and without NO treatment both showed intermediate values between those observed in green and red peppers, although the value in NO-treated fruits was lower than in BP untreated fruits. The O-generating NADPH oxidase isozymes I and VI were the most affected. On the other hand, four SOD isozymes were identified by non-denaturing electrophoresis: one Mn-SOD, one Fe-SOD, and two CuZn-SODs. However, none of these SOD isozymes showed any significant change during the ripening from green to red fruits or under NO treatment. In contrast, at the molecular level, both RNA-sequencing and real-time quantitative PCR analyses revealed different patterns with downregulation of four genes RBOH A, C, D, and E during pepper fruit ripening. On the contrary, it was found out the upregulation of a Mn-SOD gene in the ripening transition from immature green to red ripe stages, whereas a Fe-SOD gene was downregulated. In summary, the data reveal a contradictory behavior between activity and gene expression of the enzymes involved in the metabolism of O during the ripening of pepper fruit. However, it could be concluded that the prevalence and regulation of the O generation system (NADPH oxidase-like) seem to be essential for an appropriate control of the pepper fruit ripening, which, additionally, is modulated in the presence of a NO-enriched environment.The research work of FC and JP is supported by a European Regional Development Fund-cofinanced grant from the Ministry of Economy and Competitiveness (AGL2015-65104-P and PID2019-103924GB-I00), the Plan Andaluz de Investigación, Desarrollo e Innovación (PAIDI 2020) (P18-FR-1359), and Junta de Andalucía (group BIO192), Spain.Frontiers MediaEuropean CommissionMinisterio de Economía y Competitividad (España)Junta de AndalucíaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2020202020202020info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/218088reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2015-65104-Pinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-103924GB-I00http://dx.doi.org/10.3389/fpls.2020.00485Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2180882026-05-22T06:33:51Z
dc.title.none.fl_str_mv Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
title Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
spellingShingle Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
González-Gordo, Salvador
NADPH oxidase
Nitric oxide
Nitration
Pepper fruit
Respiratory burst oxidase homolog
S-nitrosation
Superoxide dismutase
Ripening
title_short Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
title_full Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
title_fullStr Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
title_full_unstemmed Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
title_sort Superoxide radical metabolism in sweet pepper (Capsicum annuum L.) fruits Is regulated by ripening and by a NO-enriched environment
dc.creator.none.fl_str_mv González-Gordo, Salvador
Rodríguez-Ruiz, Marta
Palma Martínez, José Manuel
Corpas, Francisco J.
author González-Gordo, Salvador
author_facet González-Gordo, Salvador
Rodríguez-Ruiz, Marta
Palma Martínez, José Manuel
Corpas, Francisco J.
author_role author
author2 Rodríguez-Ruiz, Marta
Palma Martínez, José Manuel
Corpas, Francisco J.
author2_role author
author
author
dc.contributor.none.fl_str_mv European Commission
Ministerio de Economía y Competitividad (España)
Junta de Andalucía
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv NADPH oxidase
Nitric oxide
Nitration
Pepper fruit
Respiratory burst oxidase homolog
S-nitrosation
Superoxide dismutase
Ripening
topic NADPH oxidase
Nitric oxide
Nitration
Pepper fruit
Respiratory burst oxidase homolog
S-nitrosation
Superoxide dismutase
Ripening
description Superoxide radical (O) is involved in numerous physiological and stress processes in higher plants. Fruit ripening encompasses degradative and biosynthetic pathways including reactive oxygen and nitrogen species. With the use of sweet pepper (Capsicum annuum L.) fruits at different ripening stages and under a nitric oxide (NO)-enriched environment, the metabolism of O was evaluated at biochemical and molecular levels considering the O generation by a NADPH oxidase system and its dismutation by superoxide dismutase (SOD). At the biochemical level, seven O-generating NADPH-dependent oxidase isozymes [also called respiratory burst oxidase homologs (RBOHs) I–VII], with different electrophoretic mobility and abundance, were detected considering all ripening stages from green to red fruits and NO environment. Globally, this system was gradually increased from green to red stage with a maximum of approximately 2.4-fold increase in red fruit compared with green fruit. Significantly, breaking-point (BP) fruits with and without NO treatment both showed intermediate values between those observed in green and red peppers, although the value in NO-treated fruits was lower than in BP untreated fruits. The O-generating NADPH oxidase isozymes I and VI were the most affected. On the other hand, four SOD isozymes were identified by non-denaturing electrophoresis: one Mn-SOD, one Fe-SOD, and two CuZn-SODs. However, none of these SOD isozymes showed any significant change during the ripening from green to red fruits or under NO treatment. In contrast, at the molecular level, both RNA-sequencing and real-time quantitative PCR analyses revealed different patterns with downregulation of four genes RBOH A, C, D, and E during pepper fruit ripening. On the contrary, it was found out the upregulation of a Mn-SOD gene in the ripening transition from immature green to red ripe stages, whereas a Fe-SOD gene was downregulated. In summary, the data reveal a contradictory behavior between activity and gene expression of the enzymes involved in the metabolism of O during the ripening of pepper fruit. However, it could be concluded that the prevalence and regulation of the O generation system (NADPH oxidase-like) seem to be essential for an appropriate control of the pepper fruit ripening, which, additionally, is modulated in the presence of a NO-enriched environment.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
2020
2020
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/10261/218088
url http://hdl.handle.net/10261/218088
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2015-65104-P
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-103924GB-I00
http://dx.doi.org/10.3389/fpls.2020.00485
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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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