A new oxidative pathway of nitric oxide production from oximes in plants

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dc.contributor.authorLópez Gómez, Pedro
dc.contributor.authorBuezo Bravo, Javier
dc.contributor.authorUrra Rodríguez, Marina
dc.contributor.authorCornejo Ibergallartu, Alfonso
dc.contributor.authorEsteban Terradillos, Raquel
dc.contributor.authorFernández de los Reyes, Jorge
dc.contributor.authorUrarte Rodríguez, Estíbaliz
dc.contributor.authorRodríguez-Dobreva, Estefanía
dc.contributor.authorChamizo Ampudia, Alejandro
dc.contributor.authorEguaras, Alejandro
dc.contributor.authorWolf, Sebastian
dc.contributor.authorMarino Bilbao, Daniel
dc.contributor.authorMartínez Merino, Víctor
dc.contributor.authorMorán Juez, José Fernando
dc.contributor.departmentCienciases_ES
dc.contributor.departmentZientziakeu
dc.contributor.departmentInstitute for Multidisciplinary Research in Applied Biology - IMABen
dc.contributor.departmentInstitute for Advanced Materials and Mathematics - INAMAT2en
dc.date.accessioned2024-02-13T16:02:16Z
dc.date.issued2024
dc.date.updated2024-02-13T15:27:11Z
dc.description.abstractNitric oxide (NO) is an essential reactive oxygen species and a signal molecule in plants. Although several studies have proposed the occurrence of oxidative NO production, only reductive routes for NO production, such as the nitrate (NO-3) -upper-reductase pathway, have been evidenced to date in land plants. However, plants grown axenically with ammonium as the sole source of nitrogen exhibit contents of nitrite and NO3, evidencing the existence of a metabolic pathway for oxidative production of NO. We hypothesized that ox- imes, such as indole-3-acetaldoxime (IAOx), a precursor to indole-3-acetic acid, are intermediate oxidation products in NO synthesis. We detected the production of NO from IAOx and other oximes catalyzed by peroxidase (POD) enzyme using both 4-amino-5-methylamino-20,70-difluorescein fluorescence and chem- iluminescence. Flavins stimulated the reaction, while superoxide dismutase inhibited it. Interestingly, mouse NO synthase can also use IAOx to produce NO at a lower rate than POD. We provided a full mech- anism for POD-dependent NO production from IAOx consistent with the experimental data and supported by density functional theory calculations. We showed that the addition of IAOx to extracts from Medicago truncatula increased the in vitro production of NO, while in vivo supplementation of IAOx and other oximes increased the number of lateral roots, as shown for NO donors, and a more than 10-fold increase in IAOx dehydratase expression. Furthermore, we found that in vivo supplementation of IAOx increased NO pro- duction in Arabidopsis thaliana wild-type plants, while prx33-34 mutant plants, defective in POD33-34, had reduced production. Our data show that the release of NO by IAOx, as well as its auxinic effect, explain the superroot phenotype. Collectively, our study reveals that plants produce NO utilizing diverse molecules such as oximes, POD, and flavins, which are widely distributed in the plant kingdom, thus intro- ducing a long-awaited oxidative pathway to NO production in plants. This knowledge has essential impli- cations for understanding signaling in biological systems.en
dc.description.sponsorshipThis work was supported by grants AGL2014-52396, AGL2017-86293-P, and PID2022-142968NB-I00 from MCIN/AEI/10.13039/501100011033/ FEDER, UE, and a grant from the Public University of Navarre (PID2020-117703GB-I00) (to J.F.M.) and the UPV/EHU-GV IT-1018-16 program (Basque Government) (to R.E.). M.U. is a recipient of a predoctoral fellowship from the Government of Navarre, Spain. J.B. and P.L.-G. have received pre-doctoral fellowships from the Public University of Navarre, Spain. P.L.-G. is currently financed by a postdoctoral contract funded by the Spanish National Research Council (20224AT017). J.B. is also a recipient of the ‘‘Requalification of the Spanish University System for 2021-2023, Public University of Navarra’’ fellowship, funded by the European Union-Next Generation (EU).en
dc.embargo.inicio2024-02-13
dc.embargo.lift2025-01-01
dc.embargo.terms2025-01-01
dc.format.mimetypeapplication/pdfen
dc.format.mimetypeapplication/zipen
dc.identifier.citationLópez-Gómez, P., Buezo, J., Urra, M., Cornejo, A., Esteban, R., Fernández de los Reyes, J., Urarte, E., Rodríguez-Dobreva, E., Chamizo-Ampudia, A., Eguaras, A., Wolf, S., Marino, D., Martínez-Merino, V., Moran, J.F. (2024) A new oxidative pathway of nitric oxide production from oximes in plants. Molecular Plant, (17), 178-198. https://doi.org/10.1016/j.molp.2023.12.009.en
dc.identifier.doi10.1016/j.molp.2023.12.009
dc.identifier.issn1674-2052
dc.identifier.urihttps://academica-e.unavarra.es/handle/2454/47486
dc.language.isoengen
dc.publisherCell Pressen
dc.relation.ispartofMolecular Plant 17(1), 2024, 178-198en
dc.relation.projectIDinfo:eu-repo/grantAgreement/MINECO//AGL2014-52396-P/ES/
dc.relation.projectIDinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2017-86293-P/ES/
dc.relation.projectIDinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-142968NB-I00/ES/
dc.relation.publisherversionhttps://doi.org/10.1016/j.molp.2023.12.009
dc.rights© 2023 The Authors.en
dc.rights.accessRightsinfo:eu-repo/semantics/openAccess
dc.subjectAmmonium oxidationen
dc.subjectAuxinen
dc.subjectNitric oxideen
dc.subjectOximeen
dc.subjectPeroxidaseen
dc.subjectRoot phenotypeen
dc.titleA new oxidative pathway of nitric oxide production from oximes in plantsen
dc.typeinfo:eu-repo/semantics/article
dc.type.versioninfo:eu-repo/semantics/acceptedVersion
dspace.entity.typePublication
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relation.isAuthorOfPublication.latestForDiscovery2e02a0e9-6882-4ace-9d18-07f7043e276e

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