A new oxidative pathway of nitric oxide production from oximes in plants
Consultable a partir de
2025-01-01
Fecha
2024Autor
Versión
Acceso embargado / Sarbidea bahitua dago
Tipo
Artículo / Artikulua
Versión
Versión aceptada / Onetsi den bertsioa
Identificador del proyecto
Impacto
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10.1016/j.molp.2023.12.009
Resumen
Nitric 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 ...
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Nitric 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. [--]
Materias
Ammonium oxidation,
Auxin,
Nitric oxide,
Oxime,
Peroxidase,
Root phenotype
Editor
Cell Press
Publicado en
Molecular Plant 17(1), 2024, 178-198
Departamento
Universidad Pública de Navarra. Departamento de Ciencias /
Nafarroako Unibertsitate Publikoa. Zientziak Saila /
Universidad Pública de Navarra/Nafarroako Unibertsitate Publikoa. Institute for Multidisciplinary Research in Applied Biology - IMAB /
Universidad Pública de Navarra/Nafarroako Unibertsitate Publikoa. Institute for Advanced Materials and Mathematics - INAMAT2
Versión del editor
Entidades Financiadoras
This 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).