Person: Morán Juez, José Fernando
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Morán Juez
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José Fernando
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Ciencias
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IMAB. Research Institute for Multidisciplinary Applied Biology
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0000-0001-6621-6961
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Publication Open Access The proteome of Medicago truncatula in response to ammonium and urea nutrition reveals the role of membrane proteins and enzymes of root lignification(Elsevier, 2019) Royo Castillejo, Beatriz; Esteban Terradillos, Raquel; Buezo Bravo, Javier; Santamaría Martínez, Enrique; Fernández Irigoyen, Joaquín; Becker, Dirk; Morán Juez, José Fernando; Zientziak; Institute for Multidisciplinary Research in Applied Biology - IMAB; Ciencias; Universidad Pública de Navarra / Nafarroako Unibertsitate PublikoaPlants differ widely in their growth and tolerance responses to ammonium and urea nutrition, while derived phenotypes seem markedly different from plants grown under nitrate supply. Plant responses to N sources are complex, and the traits involved remain unknown. This work reports a comprehensive and quantitative root proteomic study on the NH4+-tolerant legume Medicago truncatula grown under axenic conditions with either nitrate, NH4+ or urea supply as sole N source by using the iTRAQ method. Sixty-one different proteins among the three N sources were identified. Interestingly, among the proteomic responses, urea nutrition displayed greater similarity to nitrate than to ammonium nutrition. We found remarkable differences in membrane proteins that play roles in sensing the N form, and regulate the intracellular pH and the uptake of N. Also, several groups of proteins were differentially expressed in the C metabolism pathway involved in reorganizing N assimilation. In addition, enzymes related to phenylpropanoid metabolism, including the peroxidases POD2, POD6, POD7 and POD11, which were up-regulated under ammonium nutrition, contributed to the reinforcement of cell walls, as confirmed by specific staining of lignin. Thus, we identified cell wall lignification as an important tolerance mechanism of root cells associated with the stunted phenotype typical of plants grown under ammonium nutrition.Publication Open Access Drought tolerance response of high-yielding soybean varieties to mild drought: physiological and photochemical adjustments(Wiley, 2019) Buezo Bravo, Javier; Sanz Sáez, Álvaro; Morán Juez, José Fernando; Soba Hidalgo, David; Aranjuelo Michelena, Iker; Esteban Terradillos, Raquel; Ciencias; Zientziak; Universidad Pública de Navarra / Nafarroako Unibertsitate PublikoaSoybean is a crop of agronomic importance that requires adequate watering during its growth to achieve high production. In this study, we determined physiological, photochemical and metabolic differences in five soybean varieties selected from the parental lines of a nested association mapping population during mild drought. These varieties have been described as high yielding (NE3001, HY1; LD01-5907, HY2) or drought tolerant (PI518751; HYD1; PI398881, HYD2). Nevertheless, there has been little research on the physiological traits that sustain their high productivity under water-limited conditions. The results indicate that high-yielding varieties under drought cope with the shortage of water by enhancing their photoprotective defences and invest in growth and productivity, linked to a higher intrinsic water use efficiency. This is the case of the variety N-3001 (HY1), with a tolerance strategy involving a faster transition into the reproductive stage to avoid the drought period. The present study highlights the role of the physiological and biochemical adjustments of various soybean varieties to cope with water-limited conditions. Moreover, the obtained results underscore the fact that the high phenotypic plasticity among soybean phenotypes should be exploited to compensate for the low genetic variability of this species when selecting plant productivity in constrained environments.Publication Open Access Comparison of four functionalization methods of gold nanoparticles for enhancing the enzyme-linked immunosorbent assay (ELISA)(Beilstein-Institut, 2017) Ciáurriz Gortari, Paula; Fernández Santos, Fátima; Tellechea Malda, Edurne; Morán Juez, José Fernando; Asensio, Aarón C.; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako Institutua; Gobierno de Navarra / Nafarroako Gobernua, proyecto SABioDThe enzyme-linked immunosorbent assay (ELISA) technique is based on the specific recognition ability of the molecular structure of an antigen (epitope) by an antibody and is likely the most important diagnostic technique used today in bioscience. With this methodology, it is possible to diagnose illness, allergies, alimentary fraud, and even to detect small molecules such as toxins, pesticides, heavy metals, etc. For this reason, any procedures that improve the detection limit, sensitivity or reduce the analysis time could have an important impact in several fields. In this respect, many methods have been developed for improving the technique, ranging from fluorescence substrates to methods for increasing the number of enzyme molecules involved in the detection such as the biotin–streptavidin method. In this context, nanotechnology has offered a significant number of proposed solutions, mainly based on the functionalization of nanoparticles from gold to carbon which could be used as antibody carriers as well as reporter enzymes like peroxidase. However, few works have focused on the study of best practices for nanoparticle functionalization for ELISA enhancement. In this work, we use 20 nm gold nanoparticles (AuNPs) as a vehicle for secondary antibodies and peroxidase (HRP). The design of experiments technique (DOE) and four different methods for biomolecule loading were compared using a rabbit IgG/goat anti-rabbit IgG ELISA model (adsorption, directional, covalent and a combination thereof). As a result, AuNP probes prepared by direct adsorption were the most effective method. AuNPs probes were then used to detect gliadin, one of the main components of wheat gluten, the protein composite that causes celiac disease. With this optimized approach, our data showed a sensitivity increase of at least five times and a lower detection limit with respect to a standard ELISA of at least three times. Additionally, the assay time was remarkably decreased.Publication Open Access Tryptophan levels as a marker of auxins and nitric oxide signaling(MDPI, 2022) López Gómez, Pedro; Smith, Edward N.; Bota, Pedro; Cornejo Ibergallartu, Alfonso; Urra Rodríguez, Marina; Buezo Bravo, Javier; Morán Juez, José Fernando; Zientziak; Institute for Advanced Materials and Mathematics - INAMAT2; Institute for Multidisciplinary Research in Applied Biology - IMAB; Ciencias; Gobierno de Navarra / Nafarroako Gobernua; Universidad Pública de Navarra / Nafarroako Unibertsitate PublikoaThe aromatic amino acid tryptophan is the main precursor for indole-3-acetic acid (IAA), which involves various parallel routes in plants, with indole-3-acetaldoxime (IAOx) being one of the most common intermediates. Auxin signaling is well known to interact with free radical nitric oxide (NO) to perform a more complex effect, including the regulation of root organogenesis and nitrogen nutrition. To fathom the link between IAA and NO, we use a metabolomic approach to analyze the contents of low-molecular-mass molecules in cultured cells of Arabidopsis thaliana after the application of S-nitrosoglutathione (GSNO), an NO donor or IAOx. We separated the crude extracts of the plant cells through ion-exchange columns, and subsequent fractions were analyzed by gas chromatography-mass spectrometry (GC-MS), thus identifying 26 compounds. A principal component analysis (PCA) was performed on N-metabolism-related compounds, as classified by the Kyoto Encyclopedia of Genes and Genomes (KEGG). The differences observed between controls and treatments are mainly explained by the differences in Trp contents, which are much higher in controls. Thus, the Trp is a shared response in both auxin- and NO-mediated signaling, evidencing some common signaling mechanism to both GSNO and IAOx. The differences in the low-molecularmass- identified compounds between GSNO- and IAOx-treated cells are mainly explained by their concentrations in benzenepropanoic acid, which is highly associated with IAA levels, and salicylic acid, which is related to glutathione. These results show that the contents in Trp can be a marker for the study of auxin and NO signaling.Publication Open Access Nitric oxide induces the alternative oxidase pathway in Arabidopsis seedlings deprived of inorganic phosphate(Oxford University Press, 2015) Royo Castillejo, Beatriz; Morán Juez, José Fernando; Ratcliffe, R. George; Gupta, Kapuganti J.; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaPhosphate starvation compromises electron flow through the cytochrome pathway of the mitochondrial electron transport chain, and plants commonly respond to phosphate deprivation by increasing flow through the alternative oxidase (AOX). To test whether this response is linked to the increase in nitric oxide (NO) production that also increases under phosphate starvation, Arabidopsis thaliana seedlings were grown for 15 d on media containing either 0 or 1mM inorganic phosphate. The effects of the phosphate supply on growth, the production of NO, respiration, the AOX level and the production of superoxide were compared for wild-type (WT) seedlings and the nitrate reductase double mutant nia. Phosphate deprivation increased NO production in WT roots, and the AOX level and the capacity of the alternative pathway to consume electrons in WT seedlings; whereas the same treatment failed to stimulate NO production and AOX expression in the nia mutant, and the plants had an altered growth phenotype. The NO donor S-nitrosoglutathione rescued the growth phenotype of the nia mutants under phosphate deprivation to some extent, and it also increased the respiratory capacity of AOX. It is concluded that NO is required for the induction of the AOX pathway when seedlings are grown under phosphate-limiting conditions.Publication Open Access IAOx induces the SUR phenotype and differential signalling from IAA under different types of nitrogen nutrition in Medicago truncatula roots(Elsevier, 2019) Buezo Bravo, Javier; Esteban Terradillos, Raquel; Cornejo Ibergallartu, Alfonso; López Gómez, Pedro; Marino Bilbao, Daniel; Chamizo Ampudia, Alejandro; Gil Idoate, María José; Martínez Merino, Víctor; Morán Juez, José Fernando; Zientziak; Institute for Multidisciplinary Research in Applied Biology - IMAB; Institute for Advanced Materials and Mathematics - INAMAT2; Ciencias; Universidad Pública de Navarra / Nafarroako Unibertsitate PublikoaIndole-3-acetaldoxime (IAOx) is a particularly relevant molecule as an intermediate in the pathway for tryptophan-dependent auxin biosynthesis. The role of IAOx in growth-signalling and root phenotype is poorly studied in cruciferous plants and mostly unknown in non-cruciferous plants. We synthesized IAOx and applied it to M. truncatula plants grown axenically with NO3-, NH4+ or urea as the sole nitrogen source. During 14 days of growth, we demonstrated that IAOx induced an increase in the number of lateral roots, especially under NH4+ nutrition, while elongation of the main root was inhibited. This phenotype is similar to the phenotype known as “superroot” previously described in SUR1- and SUR2-defective Arabidopsis mutants. The effect of IAOx, IAA or the combination of both on the root phenotype was different and dependent on the type of N-nutrition. Our results also showed the endogenous importance of IAOx in a legume plant in relation to IAA metabolism, and suggested IAOx long-distance transport depending on the nitrogen source provided. Finally, our results point out to CYP71A as the major responsible enzymes for IAA synthesis from IAOx.Publication Open Access Both free indole-3-acetic acid and photosynthetic performance are important players in the response of Medicago truncatula to urea and ammonium nutrition under axenic conditions(Frontiers Media, 2016) Esteban Terradillos, Raquel; Royo Castillejo, Beatriz; Urarte Rodríguez, Estíbaliz; Zamarreño, Ángel M.; García Mina, José M.; Morán Juez, José Fernando; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaWe aimed to identify the early stress response and plant performance of Medicago truncatula growing in axenic medium with ammonium or urea as the sole source of nitrogen, with respect to nitrate-based nutrition. Biomass measurements, auxin content analyses, root system architecture (RSA) response analyses, and physiological parameters were determined. Both ammonium and ureic nutrition severely affected the RSA, resulting in changes in the main elongation rate, lateral root development, and insert position from the root base. The auxin content decreased in both urea- and ammonium-treated roots; however, only the ammonium-treated plants were affected at the shoot level. The analysis of chlorophyll a fluorescence transients showed that ammonium affected photosystem II, but urea did not impair photosynthetic activity. Superoxide dismutase isoenzymes in the plastids were moderately affected by urea and ammonium in the roots. Overall, our results showed that low N doses from different sources had no remarkable effects on M. truncatula, with the exception of the differential phenotypic root response. High doses of both ammonium and urea caused great changes in plant length, auxin contents and physiological measurements. Interesting correlations were found between the shoot auxin pool and both plant length and the “performance index” parameter, which is obtained from measurements of the kinetics of chlorophyll a fluorescence. Taken together, these data demonstrate that both the indole-3-acetic acid pool and performance index are important components of the response of M. truncatula under ammonium or urea as the sole N source.Publication Open Access Depletion of the heaviest stable N isotope is associated with NH4+/NH3 toxicity in NH4+-fed plants(BioMed Central, 2011) Ariz Arnedo, Idoia; Cruz, Cristina; Morán Juez, José Fernando; González Moro, María Begoña; García Olaverri, Carmen; González Murua, Carmen; Martins Loucao, María A.; Aparicio Tejo, Pedro María; Estatistika eta Ikerketa Operatiboa; Estadística e Investigación Operativa; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaBackground: In plants, nitrate (NO3-) nutrition gives rise to a natural N isotopic signature (δ15N), which correlates with the δ15N of the N source. However, little is known about the relationship between the δ15N of the N source and the 14N/15N fractionation in plants under ammonium (NH4+) nutrition. When NH4 + is the major N source, the two forms, NH4 + and NH3, are present in the nutrient solution. There is a 1.025 thermodynamic isotope effect between NH3 (g) and NH4 + (aq) which drives to a different δ15N. Nine plant species with different NH4 +-sensitivities were cultured hydroponically with NO3 - or NH4 + as the sole N sources, and plant growth and δ15N were determined. Short-term NH4 +/NH3 uptake experiments at pH 6.0 and 9.0 (which favours NH3 form) were carried out in order to support and substantiate our hypothesis. N source fractionation throughout the whole plant was interpreted on the basis of the relative transport of NH4 + and NH3. Results: Several NO3 --fed plants were consistently enriched in 15N, whereas plants under NH4 + nutrition were depleted of 15N. It was shown that more sensitive plants to NH4 + toxicity were the most depleted in 15N. In parallel, N-deficient pea and spinach plants fed with 15NH4 + showed an increased level of NH3 uptake at alkaline pH that was related to the 15N depletion of the plant. Tolerant to NH4 + pea plants or sensitive spinach plants showed similar trend on 15N depletion while slight differences in the time kinetics were observed during the initial stages. The use of RbNO3 as control discarded that the differences observed arise from pH detrimental effects. Conclusions: This article proposes that the negative values of δ15N in NH4 +-fed plants are originated from NH3 uptake by plants. Moreover, this depletion of the heavier N isotope is proportional to the NH4 +/NH3 toxicity in plants species. Therefore, we hypothesise that the low affinity transport system for NH4 + may have two components: one that transports N in the molecular form and is associated with fractionation and another that transports N in the ionic form and is not associated with fractionation.Publication Open Access Soybean dihydrolipoamide dehydrogenase (ferric leghemoglobin reductase 2) interacts with and reduces ferric rice non-symbiotic hemoglobin 1(Simplex Academic Publishers, 2013) Gopalasubramaniama, Sabarinathan K.; Kondapallib, Kalyan C.; Millán-Pacheco, César; Pastor, Nina; Stemmler, Timothy L.; Morán Juez, José Fernando; Arredondo-Peter, Raúl; Ciencias del Medio Natural; Natura Ingurunearen Zientziak; Gobierno de Navarra / Nafarroako GobernuaFerrous oxygenated hemoglobins (Hb2+O2) autoxidize to ferric Hb3+, but Hb3+ is reduced to Hb2+ by enzymatic and non-enzymatic mechanisms. We characterized the interaction between the soybean ferric leghemoglobin reductase 2 (FLbR2) and ferric rice non-symbiotic Hb1 (Hb13+). Spectroscopic analysis showed that FLbR2 reduces Hb13+. Analysis by tryptophan fluorescence quenching showed that FLbR2 interacts with Hb13+, however the use of ITC and IEF techniques revealed that this interaction is weak. In silico modeling showed that predicted FLbR2 and native Hb13+ interact at the FAD-binding domain of FLbR2 and the CD-loop and helix F of Hb13+.Publication Embargo A new oxidative pathway of nitric oxide production from oximes in plants(Cell Press, 2024) López Gómez, Pedro; Buezo Bravo, Javier; Urra Rodríguez, Marina; Cornejo Ibergallartu, Alfonso; Esteban Terradillos, Raquel; Fernández de los Reyes, Jorge; Urarte Rodríguez, Estíbaliz; Rodríguez-Dobreva, Estefanía; Chamizo Ampudia, Alejandro; Eguaras, Alejandro; Wolf, Sebastian; Marino Bilbao, Daniel; Martínez Merino, Víctor; Morán Juez, José Fernando; Ciencias; Zientziak; Institute for Multidisciplinary Research in Applied Biology - IMAB; Institute for Advanced Materials and Mathematics - INAMAT2Nitric 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.