Browsing by Author "Esteban Terradillos, Raquel"
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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 Embargo Downed woody debris carbon emissions in a European temperate virgin forest as driven by species, decay classes, diameter and microclimate(Elsevier, 2024-02-20) Buezo Bravo, Javier; Medina, Nagore G.; Hereş, Ana-Maria; Petritan, Ion C.; Cornelissen, Johannes H.C.; Petritan, Any Mary; Esteban Terradillos, Raquel; Ilinca, Elisabeth; Stoian, R.; Curiel Yuste, Jorge; Ciencias; Zientziak; Institute for Multidisciplinary Research in Applied Biology - IMABDowned woody debris (DWD) plays an important role as regulator of nutrient and carbon (C) cycling in forests, accounting for up to the 20 % of the total C stocks in primary forests. DWD persistence is highly influenced by microbial decomposition, which is determined by various environmental factors, including fluctuations in temperature and moisture, as well as in intrinsic DWD properties determined by species, diameter, or decay classes (DCs). The relative importance of these different drivers, as well as their interactions, remains largely unknown. Moreover, the importance of DWD for C cycling in virgin forests remains poorly understood, due to their scarcity and poor accessibility. To address this research gap, we conducted a study on DWD respiration (RDWD), in a temperate virgin forest dominated by European beech and silver fir. Our investigation analysed the correlation between RDWD of these two dominant tree species and the seasonal changes in climate (temperature and moisture), considering other intrinsic DWD traits such as DCs (1, 2 and 4) and diameters (1, 10 and 25 cm). As anticipated, RDWD (normalized per gram of dry DWD) increased with air temperature. Surprisingly, DWD diameter also had a strong positive correlation with R DWD. Nonetheless, the sensitivity to both variables and other intrinsic traits (DC and density) was greatly modulated by the species. On the contrary, water content, which exhibited a considerable spatial variation, had an overall negative effect on R DWD. Virgin forests are generally seen as ineffective C sinks due to their lack of net productivity and high respiration and nutrient turnover. However, the rates of R DWD in this virgin forest were significantly lower than those previously estimated for managed forests. This suggests that DWD in virgin forests may be bufferingforest CO2 emissions to the atmosphere more than previously thought.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 Ecophysiological roles of abaxial anthocyanins in a perennial understorey herb from temperate deciduous forests(Oxford University Press, 2015) Fernández Marín, Beatriz; Esteban Terradillos, Raquel; Míguez, Fátima; Artetxe, Unai; Castañeda Presa, Verónica; Pintó Marijuan, Marta; Becerril, José María; García Plazaola, José Ignacio; Natura Ingurunearen Zientziak; Ciencias del Medio Natural; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaAccumulation of abaxial anthocyanins is an intriguing leaf trait particularly common among deeply shaded understorey plants of tropical and temperate forests whose ecological significance is still not properly understood. To shed light on it, possible ecophysiological roles of abaxial anthocyanins were tested in the perennial understorey herb of temperate deciduous forests Saxifraga hirsuta, chosen as a model species due to the coexistence of green and anthocyanic leaves and the presence of an easily removable lower anthocyanic epidermis. Anthocyanins accumulated during autumn, which temporally matched the overstorey leaf fall. Patterns of development of abaxial anthocyanins and direct measurements of photochemical efficiency under monochromatic light were not consistent with a photoprotective hypothesis. Enhancement of light capture also seemed unlikely since the back-scattering of red light towards the lower mesophyll was negligible. Seed germination was similar under acyanic and anthocyanic leaves. A relevant consequence of abaxial anthocyanins was the dramatic reduction of light transmission through the leaf. The dark environment generated underneath the Saxifraga canopy was enhanced by the horizontal repositioning of leaves, which occurs in parallel with reddening. This might play a role in biotic interactions by inhibiting vital processes of competitors, which may be of especial importance in spring before the overstorey leaves sprout.Publication Open Access Established and proposed roles of xanthine oxidoreductase in oxidative and reductive pathways in plants(Springer, 2014) Urarte Rodríguez, Estíbaliz; Esteban Terradillos, Raquel; Morán Juez, José Fernando; Bittner, Florian; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaXanthine oxidoreductase (XOR) is among the most-intensively studied enzymes known to participate in the consumption of oxygen in cells. However, it attracted the attention of researchers due its participation in free radical production in vivo, mainly through the production of superoxide radicals. In plants, XOR is a key enzyme in purine degradation where it catalyzes the oxidation of hypoxanthine to xanthine and of xanthine to uric acid. Both reactions are accompanied by electron transfer to either NAD+ with simultaneous formation of NADH or to molecular oxygen, which results in formation of superoxides. Characterization of plant XOR mutants and isolated XOR proteins from various plant species provided evidence that the enzyme plays significant roles in plant growth, leaf senescence, fruit size, synthesis of nitrogen storage compounds, and plant-pathogen interactions. Moreover, the ability of XOR to carry out redox reactions as NADH oxidase and to produce reactive oxygen species and nitric oxide, together with a possible complementary role in abscisic acid synthesis have raised further attention on the importance of this enzyme. Based on these established and proposed functions, XOR is discussed as regulator of different processes of interest in plant biology and agriculture.Publication Open Access Foliar heavy metals and stable isotope (δ13C, δ15N) profiles as reliable urban pollution biomonitoring tools(Elsevier, 2021) Soba Hidalgo, David; Gámez Guzmán, Angie Lorena; Úriz, Naroa; Ruiz de Larrinaga, Lorena; González Murua, Carmen; Becerril, José María; Esteban Terradillos, Raquel; Serret, Dolors; Araus, José Luis; Aranjuelo Michelena, Iker; Agronomía, Biotecnología y Alimentación; Agronomia, Bioteknologia eta ElikaduraAnthropogenic heavy metal pollution is an important health issue in urban areas, and therefore rapid and inexpensive monitoring in time and space is desirable. This study aimed (i) to assess the suitability of Tilia cordata leaves as a valuable heavy metal bioindicator, including seasonal changes in concentrations and (ii) to evaluate the use of leaf carbon and nitrogen isotope composition (δ13C and δ15N) as novel indicators of urban heavy metal pollution. Leaves were collected from three different pollution intensity locations (Bilbao, Vitoria, and Muskiz) in the Basque Country (northern Spain). Analysis of leaf heavy metals related to traffic emissions and δ13C and δ15N determinations were carried out during July-October 2018. Leaf samples from Bilbao, the most populated and traffic-intense location, showed the highest concentration of heavy metals (mainly from polluted air). Additionally, the two urban areas, Bilbao and Vitoria, showed stronger correlation between these heavy metals, indicating a traffic-related source of emissions. The source of contamination (soil or air) in relation to elements and optimal sampling time is discussed herein. On the other hand, Pearson correlation analysis revealed significant trends between leaf δ13C and δ15N and the studied heavy metals, especially Pb, Cr and Cd, supporting the hypothesis of δ13C and δ15N as tools to distinguish locations according to their heavy metal pollution levels. To our knowledge, this is the first time that δ13C and δ15N have been used as monitoring tools in heavy metal pollution and consequently more research is still needed to calibrate this tool through extensive vegetation screening.Publication Open Access High irradiance induces photoprotective mechanisms and a positive effect on NH4+ stress in Pisum sativum L.(Elsevier, 2010-04-29) Ariz Arnedo, Idoia; Esteban Terradillos, Raquel; García Plazaola, José Ignacio; Becerril, José María; Aparicio Tejo, Pedro María; Morán Juez, José Fernando; Ciencias; Zientziak; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaPhotosynthesis provides plant metabolism with reduced carbon (C) but is also the main source of oxidative stress in plants. Likewise, high doses of NH4+ as sole N source have been reported to be toxic for most plants, resulting in reduced plant growth and restricting C availability. The combination of high photosynthetic photon flux densities (PPFD) and NH4+ nutrition may provide higher C availability but could also have a detrimental effect on the plants, therefore the objective of this study is to evaluate whether NH4+ induces photo-oxidative stress that is exacerbated under high light conditions. Pea plants (Pisum sativum cv. sugar-snap) were grown hydroponically with NH4+ (0.5, 2.5, 5 and 10 mM) under high (750 μmol photons m−2 s−1) or low PPFD conditions (350 μmol photons m−2 s−1). High PPFD contributes to a higher tolerance to ammonium by pea plants, as it originated higher biomass content due to higher photosynthetic rates. However, a deficit of N (0.5 and 2.5 mM NH4+) under high PPFD conditions caused an antioxidant response, as indicated by increased photoprotective pigment and chloroplastic superoxide dismutase contents. Plants grown with higher doses of N and high PPFD showed less need for photoprotection. An increase in the specific leaf weight (SLW) ratio was observed associated not only with high PPFDs but also with the highest NH4+ dose. Overall, these results demonstrate that, despite the activation of some photoprotective responses at high PPFD, there were no photoinhibitory symptoms and a positive effect on NH4+ toxicity, thus suggesting that the harmful effects of NH4+ are not directly related to the generation of photo-oxidative stress.Publication Open Access Holm oak decline is determined by shifts in fine root phenotypic plasticity in response to belowground stress(Wiley, 2022) Encinas-Valero, Manuel; Esteban Terradillos, Raquel; Hereş, Ana-Maria; Vivas, María; Fakhet, Dorra; Aranjuelo Michelena, Iker; Solla, Alejandro; Moreno, Gerardo; Curiel Yuste, Jorge; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaClimate change and pathogen outbreaks are the two major causes of decline in Mediterranean holm oak trees (Quercus ilex L. subsp. ballota (Desf.) Samp.). Crown-level changes in response to these stressful conditions have been widely documented but the responses of the root systems remain unexplored. The effects of environmental stress over roots and its potential role during the declining process need to be evaluated. We aimed to study how key morphological and architectural root parameters and nonstructural carbohydrates of roots are affected along a holm oak health gradient (i.e. within healthy, susceptible and declining trees). Holm oaks with different health statuses had different soil resource-uptake strategies. While healthy and susceptible trees showed a conservative resource-uptake strategy independently of soil nutrient availability, declining trees optimized soil resource acquisition by increasing the phenotypic plasticity of their fine root system. This increase in fine root phenotypic plasticity in declining holm oaks represents an energy-consuming strategy promoted to cope with the stress and at the expense of foliage maintenance. Our study describes a potential feedback loop resulting from strong unprecedented belowground stress that ultimately may lead to poor adaptation and tree death in the Spanish dehesa.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 The importance of the urea cycle and its relationships to polyamine metabolism during ammonium stress in Medicago truncatula(Oxford University Press, 2022) Urra Rodríguez, Marina; Buezo Bravo, Javier; Royo Castillejo, Beatriz; Cornejo Ibergallartu, Alfonso; López Gómez, Pedro; Cerdán Ruiz, Daniel; Esteban Terradillos, Raquel; Martínez Merino, Víctor; Gogorcena, Yolanda; Tavladoraki, Paraskevi; Morán Juez, José Fernando; Ciencias; Zientziak; Institute for Advanced Materials and Mathematics - INAMAT2; Institute for Multidisciplinary Research in Applied Biology - IMAB; Universidad Pública de Navarra / Nafarroako Unibertsitate Publikoa; Gobierno de Navarra / Nafarroako GobernuarenThe ornithine–urea cycle (urea cycle) makes a signifcant contribution to the metabolic responses of lower photosynthetic eukaryotes to episodes of high nitrogen availability. In this study, we compared the role of the plant urea cycle and its relationships to polyamine metabolism in ammonium-fed and nitrate-fed Medicago truncatula plants. High ammonium resulted in the accumulation of ammonium and pathway intermediates, particularly glutamine, arginine, ornithine, and putrescine. Arginine decarboxylase activity was decreased in roots, suggesting that the ornithine decarboxylase-dependent production of putrescine was important in situations of ammonium stress. The activity of copper amine oxidase, which releases ammonium from putrescine, was signifcantly decreased in both shoots and roots. In addition, physiological concentrations of ammonium inhibited copper amine oxidase activity in in vitro assays, supporting the conclusion that high ammonium accumulation favors putrescine synthesis. Moreover, early supplementation of plants with putrescine avoided ammonium toxicity. The levels of transcripts encoding urea-cyclerelated proteins were increased and transcripts involved in polyamine catabolism were decreased under high ammonium concentrations. We conclude that the urea cycle and associated polyamine metabolism function as important protective mechanisms limiting ammonium toxicity in M. truncatula. These fndings demonstrate the relevance of the urea cycle to polyamine metabolism in higher plants.Publication Open Access An integrated view of changing nutrient availability in model species: the role of signaling in the plant response(2017) Royo Castillejo, Beatriz; Morán Juez, José Fernando; Esteban Terradillos, Raquel; Ciencias del Medio Natural; Natura Ingurunearen ZientziakLas plantas tienen que hacer frente a situaciones cambiantes en cuanto a la disponibilidad de nutrientes, por ese motivo en la presente tesis se ha estudiado la respuesta de (i) Arabidopsis thaliana frente a la deficiencia de fósforo, y de (ii) Medicago truncatula expuesto a diferentes fuentes de N. En este sentido, la deficiencia de fosfato afecta al transporte de electrones mediado por el citocromo c en la cadena de transporte de electrones de la mitocondria, con lo que las plantas habitualmente aumentan el flujo de electrones a través de la oxidasa alternativa (AOX). Con el objetivo de discernir si esta respuesta está unida a un aumento en la producción de óxido rútrico (NO) bajo la deficiencia de fosfato, se crecieron axénicamente plántulas wild type (WT) y doble mutantes de la nitrato reductasa (nía) de Arabidopsis thaliana durante 15 día.s en un medio que conterúa una concentración de fosfato inorgánico de O ó 1 m vL La deficiencia de fosfato produjo un aumento de la producción de NO en las raíces WT, y a su vez también incrementó la cantidad de AOX así como la capacidad de consumir electrones de la vía alternativa en plántulas WT. Sin embargo, bajo el mismo tratamiento las mutantes nía no fueron capaces de estimular la producción de NO ni la expresión de la AOX, y como consecuencia se alteró el crecimiento de estas plántulas que exhibieron un fenotipo diferente. La adición de S nitrosoglutatión en el medio de cultivo sin fosfato, en cierto modo restituyó el fenotipo de los mutantes nia, al mismo tiempo que aumentó la capacidad respiratoria asociada a la AOX. De esta manera, se puede concluir que el NO es necesario para la inducción de la vía alternativa de respiración en situaciones en las que la disponibilidad del fosfato es limitada. En la segunda parte de esta tesis, mediante la utilización de condiciones axénicas se ha identificado la respuesta temprana así como el comportamiento de Medicago truncatuala frente a la utilización de amonio y urea como únicas fuentes de N en comparación con la nutrición nítrica. Tanto el amonio como la urea afectaron a la arquitectura radicular, observándose cambios en el ratio de crecimiento de la raíz principal, en el desarrollo de las raíces laterales, así como alternaciones en el punto de inserción de la raíz. El contenido de aminas disminuyó en raíces tratadas con amonio y urea, mientras que respecto a la parte aérea únicamente se vieron afectadas las plantas crecidas en amonio. El análisis de fluorescencia de la clorofila a mostró que mientras el aporte de amonio afectó al fotosistema II, la urea no perjudicó la actividad fotosintética. En raíces, tanto el amonio como la urea afectaron de forma moderada las isoenzimas plastidiales de la actividad superóxido dismutasa. Por otro lado, la exposición a bajas dosis (1m/M) de amonio y urea no tuvo efectos en el metabolismo ni en la señalización del N. Bajo estas condiciones, se observó una inducción de las acuaporinas así como cambios en el metabolismo de los fenilpropanoides de las raíces indicando que la absorción de N del medio por las plantas está mediada por un adecuado mecanismo de detección. Sin embargo, altas dosis (25mM) de N produjeron cambios moderados en las plantas pero no se observaron signos de toxicidad ni estrés nitro oxidativo. El contenido de aminoácidos libres y de ureidos se vio afectado a altas concentraciones de N, observándose como resultado un aumento en la producción de amidas así como la activación del ciclo GABA para compensar el exceso de N asimilado bajo nutrición amoniacal. Las raíces crecidas con amonio produjeron las mismas cantidades de NO que las raíces nítricas, indicando que dicho NO podría estar implicado en la respuesta de M. truncatula a altas concentraciones de amonio. En general, nuestros resultados indicaron que las distintas fuentes de N no tuvieron efectos remarcables en M. truncatula crecido a bajas dosis, con excepción de la distinta respuesta fenotípica encontrada en las raíces. En conjunto, estos datos demuestran que tanto el ácido 3-indolacético y el rendimiento fotosintético son componentes importantes en la respuesta de M. truncatula crecida con amonio o urea como fuentes exclusivas de N. Además, otras piezas clave en la tolerancia de M. truncatula frente a la nutrición con amonio y urea son la redistribución del N asimilado, la disponibilidad de un mecanismo de detección muy específico de la fuente de N a nivel de pared celular y membrana plasmática, así como el papel que el NO puede estar desempeñando.Publication Open Access Mechanisms of ammonium toxicity and the quest for tolerance(Elsevier, 2016) Esteban Terradillos, Raquel; Ariz Arnedo, Idoia; Cruz, Cristina; Morán Juez, José Fernando; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaAmmonium sensitivity of plants is a worldwide problem, constraining crop production. Prolonged application of ammonium as the sole nitrogen source may result in physiological and morphological disorders that lead to decreased plant growth and toxicity. The main causes of ammonium toxicity/tolerance described until now include high ammonium assimilation by plants and/or low sensitivity to external pH acidification. The various ammonium transport-related components, especially the non-electrogenic influx of NH3 (related to the depletion of 15N) and the electrogenic influx of NH4+, may contribute to ammonium accumulation, and therefore to NH3 toxicity. However, this accumulation may be influenced by increasing K+ concentration in the root medium. Recently, new insights have been provided by “omics” studies, leading to a suggested involvement of GDP mannose-pyrophosphorylase in the response pathways of NH4+ stress. In this review, we highlight the cross-talk signaling between nitrate, auxins and NO, and the importance of the connection of the plants’ urea cycle to metabolism of polyamines. Overall, the tolerance and amelioration of ammonium toxicity are outlined to improve the yield of ammonium-grown plants. This review identifies future directions of research, focusing on the putative importance of aquaporins in ammonium influx, and on genes involved in ammonium sensitivity and tolerance.Publication Open Access 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.Publication Open Access Una nueva aproximación al aprendizaje de la biología celular en Educación Secundaria(2016) Martínez Buldain, Carolina; Morán Juez, José Fernando; Esteban Terradillos, Raquel; Facultad de Ciencias Humanas y Sociales; Giza eta Gizarte Zientzien FakultateaLos sistemas educativos deben estar al servicio de la sociedad, con el fin de preparar ciudadanos cualificados para aportar y mejorar la calidad de esta. Para ello los alumnos deben adquirir una serie de competencias a través de una metodología basada en la adquisición de un aprendizaje significativo. Las ciencias en general y la biología en particular han sido herramientas fundamentales en el desarrollo humano a lo largo de la historia y por lo tanto determinantes a la hora de aportar a este fin, pero muchas veces ciertos conceptos o ideas básicas relacionadas con la biología, como la célula, resultan confusas o demasiado abstractas para alumnos de secundaria y hace que estos se desmotiven ante su estudio. Por esto, resulta imprescindible dedicar tiempo y una metodología adecuada que ayude a motivar al alumno en su aprendizaje. Este proyecto presenta una unidad didáctica dedicada a la célula con el fin de dar herramientas y facilitar el aprendizaje de este concepto.Publication Open Access Opening Pandora's box: cause and impact of errors on plant pigment studies(Frontiers Media, 2015) Fernández Marín, Beatriz; Artetxe, Unai; Barrutia, Oihana; Esteban Terradillos, Raquel; Hernández, Antonio; García Plazaola, José Ignacio; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaToday, there is an astonishing volume of scientific information available for researchers, which can be easily accessed through powerful search tools. Yet, the question now is whether all this vast amount of information is reliable. In this sense, a “bad science” controversy arose recently when many Open Access (OA) journals (more than a half) published a false, error-ridden paper, which had been submitted in order to test the publishing ethics of these journals (Bohannon, 2013). This fake article was published mainly by fraudulent journals, but it was also accepted by a number of OA journals of renowned publishers with peer-review systems. The failure to reject an article full of errors revealed that the system's gearbox is leaking somewhere. The carelessness of peer-reviews in a number of OA journals has opened a Pandora's Box, and what is more disconcerting, nobody can guarantee that it could not also affect regular journals (non OA). Traditionally, it has been assumed that scientific journals should detect and correct all these failings through the peer review before publication. Regrettably, as we show in this communication, the system is far from being perfect (Pulverer, 2010; Székely et al., 2014).Publication Embargo Oximes and nitric oxide signalling in Medicago truncatula root system architecture(2020) Buezo Bravo, Javier; Morán Juez, José Fernando; Esteban Terradillos, Raquel; Ciencias; Zientziak; Universidad Pública de Navarra / Nafarroako Unibertsitate PublikoaEl óxido nítrico (NO) es una molécula señalizadora ampliamente conocida en el mundo vegetal, relacionada con cada etapa en el desarrollo de la planta. De entre todas sus funciones descritas, se sabe que actúa sinérgicamente con el ácido indol-3-acético (IAA), promoviendo el desarrollo de raíces secundarias. Hasta ahora tan solo se han confirmado algunas vías de síntesis del NO, todas ellas reductivas, mientras que aún no se ha revelado vía oxidativa alguna. Varios informes de nuestro grupo de investigación han medido síntesis de novo de NO3- y NO2- en Pisum sativum y M. truncatula crecidas con NH4+ como única fuente de nitrógeno (datos sin publicar). Este hecho sugiere la existencia de una vía oxidativa para el NH4+ en fabáceas. Se propone también que este mismo mecanismo puede ser parte de la señalización por toxicidad de NH4+ y de los procesos para su mitigación. Dada su configuración molecular, las oximas son buenos candidatos para ser precursores del NO, y, por tanto, el primer paso de esta vía de oxidación de nitrógeno. Entre todas las oximas, la Indol-3-acetaldoxima (IAOx) es especialmente relevante ya que se sitúa en la encrucijada entre el IAA y los indol glucosinolatos. El papel del IAOx en el desarrollo y señalización está muy poco estudiado en crucíferas, y es prácticamente desconocido en otras familias. En esta tesis doctoral intentamos demostrar que el IAOx está presente en M. truncatula y que posee, además, importantes funciones de señalización durante el desarrollo radicular. Por último, hipotetizamos que la señalización de IAOx está mediada por NO. Para esta labor, hemos sintetizado IAOx y una colección de otras oximas indólicas y no indólicas puras y hemos utilizado un enfoque farmacológico utilizando la planta leguminosa modelo M. truncatula. Hemos medido el fenotipo radicular, cuantificado los compuestos indólicos en tejido (parte aérea y raíz) y medido la expresión de los genes de Indol-3-acetaldehido oxidasa e IAOx deshidratasa. Nuestros datos muestran que todas las oximas promueven el fenotipo ‘superoot’, concordando con nuestra hipótesis de que el IAOx produce su efecto a través de la liberación de NO. Este nuevo conocimiento es un gran paso hacia el descubrimiento de la vía oxidativa de síntesis de NO en plantas y arroja luz a la interacción entre IAOx, IAA y la nutrición nitrogenada, que será imprescindible para futuras investigaciones en campos de cultivoPublication Open Access El proceso investigativo como método de aprendizaje significativo: coherencia y adecuación de la propuesta en el aula de secundaria(2015) Fernández García, Gonzalo; Morán Juez, José Fernando; Esteban Terradillos, Raquel; Facultad de Ciencias Humanas y Sociales; Giza eta Gizarte Zientzien FakultateaEn este trabajo analizamos, la metodología práctica-investigativa para conocer sus beneficios para, posteriormente, realizar una reflexión de la viabilidad, coherencia y adecuación del proceso práctico en los Institutos de Secundaria atendiendo a factores como (i) el tiempo que requiere, (ii) la inversión económica necesaria, (iii) el nivel en el que se puede impartir, (iv) los contenidos curriculares que se les puede asociar y (v) la formación que requiere del profesorado. Finalmente, se contrastarán estos resultados teóricos con los resultados prácticos obtenidos en un centro de la comunidad navarra, para contrastar las hipótesis y dilucidar una respuesta a todas las dudas que atañen al proceso práctico.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 Traffic restrictions during COVID-19 lockdown improve air quality and reduce metal biodeposition in tree leaves(Elsevier, 2022) Soba Hidalgo, David; Gámez Guzmán, Angie Lorena; Becerril, José María; Esteban Terradillos, Raquel; Aranjuelo Michelena, Iker; IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako InstitutuaThe coronavirus disease (COVID-19) has had a great global impact on human health, the life of people, and economies all over the world. However, in general, COVID-19´s effect on air quality has been positive due to the restrictions on social and economic activity. This study aimed to assess the impact on air quality and metal deposition of actions taken to reduce mobility in 2020 in two different urban locations. For this purpose, we analysed air pollution (NO2, NO, NOx, SO2, CO, PM10, O3) and metal accumulation in leaves of Tilia cordata collected from April to September 2020 in two cities in northern Spain (Pamplona-PA and San Sebastián-SS). We compared their values with data from the previous year (2019) (in which there were no mobility restrictions) obtained under an identical experimental design. We found that metal accumulation was mostly lower during 2020 (compared with 2019), and lockdown caused significant reductions in urban air pollution. Nitrogen oxides decreased by 33%−44%, CO by 24%−38%, and PM10 by 16%−24%. The contents of traffic-related metals were significantly reduced in both studied cities. More specifically, significant decreases in metals related to tyre and brake wear (Zn, Fe, and Cu) and road dust resuspension (Al, Ti, Fe, Mn, and Ca) were observed. With these results, we conclude that the main reason for the improvement in urban air pollutants and metals was the reduction in the use of cars due to COVID-19 lockdown. In addition, we offer some evidence indicating the suitability of T. cordata leaves as a tool for biomonitoring metal accumulation. This information is relevant for future use by the scientific community and policy makers to implement measures to reduce traffic air pollution in urban areas and to improve environmental and human health.