Person: Marino Bilbao, Daniel
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Marino Bilbao
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Daniel
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Ciencias del Medio Natural
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0000-0002-8788-6646
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6060
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Publication Open Access Leaves play a central role in the adaptation of nitrogen and sulfur metabolism to ammonium nutrition in oilseed rape (Brassica napus)(BioMed Central, 2017) Coleto, Inmaculada; Peña, Marlon de la; Rodríguez Escalante, Jon; Bejarano, Iraide; Glauser, Gaëtan; Aparicio Tejo, Pedro María; González Moro, María Begoña; Marino Bilbao, Daniel; Ciencias del Medio Natural; Natura Ingurunearen ZientziakBackground: The coordination between nitrogen (N) and sulfur (S) assimilation is required to suitably provide plants with organic compounds essential for their development and growth. The N source induces the adaptation of many metabolic processes in plants; however, there is scarce information about the influence that it may exert on the functioning of S metabolism. The aim of this work was to provide an overview of N and S metabolism in oilseed rape (Brassica napus) when exposed to different N sources. To do so, plants were grown in hydroponic conditions with nitrate or ammonium as N source at two concentrations (0.5 and 1 mM). Results: Metabolic changes mainly occurred in leaves, where ammonium caused the up-regulation of enzymes involved in the primary assimilation of N and a general increase in the concentration of N-compounds (NH4 +, amino acids and proteins). Similarly, the activity of key enzymes of primary S assimilation and the content of S-compounds (glutathione and glucosinolates) were also higher in leaves of ammonium-fed plants. Interestingly, sulfate level was lower in leaves of ammonium-fed plants, which was accompanied by the down-regulation of SULTR1 transporters gene expression. Conclusions: The results highlight the impact of the N source on different steps of N and S metabolism in oilseed rape, notably inducing N and S assimilation in leaves, and put forward the potential of N source management to modulate the synthesis of compounds with biotechnological interest, such as glucosinolates.Publication Open Access Physiological responses of legume nodules to drought(Global Science Books, 2011) Arrese-Igor Sánchez, César; González García, Esther; Marino Bilbao, Daniel; Ladrera Fernández, Rubén; Larrainzar Rodríguez, Estíbaliz; Gil Quintana, Erena; Ciencias del Medio Natural; Natura Ingurunearen ZientziakLegumes include important agricultural crops, as their high protein content is of primary importance for human food and animal feed. In addition, the ability of most of them to establish symbiotic relationships with soil bacteria allows them to obtain their N requirements from nitrogen fixation in nodules and, therefore, avoids the use of nitrogen fertilizers. Thus, legumes are also essential to improve the soil fertility and quality of agricultural lands and to reclaim eroded or barren areas, making them crucial for agricultural and environmental sustainability. However, legume nitrogen fixation in crop species is very sensitive to environmental constraints and drought, in particular. The present contribution reviews our current knowledge on the processes involved in this inhibition, with particular emphasis on oxygen, nitrogen and carbon physiology. Emerging aspects such as oxidative damage, C/N interactions and sulphur metabolism together with future prospects are also discussed.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 Split‐root systems applied to the study of the legume‐rhizobial symbiosis: what have we learned?(Wiley, 2014) Larrainzar Rodríguez, Estíbaliz; Gil Quintana, Erena; Arrese-Igor Sánchez, César; González García, Esther; Marino Bilbao, Daniel; Ciencias del Medio Natural; Natura Ingurunearen ZientziakSplit-root system (SRS) approaches allow the differential treatment of separate and independent root systems, while sharing a common aerial part. As such, SRS is a useful tool for the discrimination of systemic (shoot origin) versus local (root/nodule origin) regulation mechanisms. This type of approach is particularly useful when studying the complex regulatory mechanisms governing the symbiosis established between legumes and Rhizobium bacteria. The current work provides an overview of the main insights gained from the application of SRS approaches to understand how nodule number (nodulation autoregulation) and nitrogen fixation are controlled both under non-stressful conditions and in response to a variety of stresses. Nodule number appears to be mainly controlled at the systemic level through a signal which is produced by nodule/root tissue, translocated to the shoot, and transmitted back to the root system, involving shoot Leu-rich repeat receptor-like kinases. In contrast, both local and systemic mechanisms have been shown to operate for the regulation of nitrogenase activity in nodules. Under drought and heavy metal stress, the regulation is mostly local, whereas the application of exogenous nitrogen seems to exert a regulation of nitrogen fixation both at the local and systemic levels.Publication Open Access Quantitative proteomics reveals the importance of nitrogen source to control glucosinolate metabolism in Arabidopsis thaliana and Brassica oleracea(Oxford University Press, 2016) Marino Bilbao, Daniel; Ariz, Idoia; Lasa Larrea, Berta; Santamaría, Enrique; Aparicio Tejo, Pedro María; Ciencias del Medio Natural; Natura Ingurunearen ZientziakAccessing different nitrogen (N) sources involves a profound adaptation of plant metabolism. In this study, a quantitative proteomic approach was used to further understand how the model plant Arabidopsis thaliana adjusts to different N sources when grown exclusively under nitrate or ammonium nutrition. Proteome data evidenced that glucosinolate metabolism was differentially regulated by the N source and that both TGG1 and TGG2 myrosinases were more abundant under ammonium nutrition, which is generally considered to be a stressful situation. Moreover, Arabidopsis plants displayed glucosinolate accumulation and induced myrosinase activity under ammonium nutrition. Interestingly, these results were also confirmed in the economically important crop broccoli (Brassica oleracea var. italica). Moreover, these metabolic changes were correlated in Arabidopsis with the differential expression of genes from the aliphatic glucosinolate metabolic pathway. This study underlines the importance of nitrogen nutrition and the potential of using ammonium as the N source in order to stimulate glucosinolate metabolism, which may have important applications not only in terms of reducing pesticide use, but also for increasing plants’ nutritional value.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.Publication Open Access A proteomic approach reveals new actors of nodule response to drought in split-root grown pea plants(Wiley, 2014) Irar, Sami; González García, Esther; Arrese-Igor Sánchez, César; Marino Bilbao, Daniel; Ciencias del Medio Natural; Natura Ingurunearen ZientziakDrought is considered the more harmful abiotic stress resulting in crops yield loss. Legumes in symbiosis with rhizobia are able to fix atmospheric nitrogen. Biological nitrogen fixation (SNF) is a very sensitive process to drought and limits legumes agricultural productivity. Several factors are known to regulate SNF including oxygen availability to bacteroids, carbon and nitrogen metabolisms; but the signalling pathways leading to SNF inhibition are largely unknown. In this work, we have performed a proteomic approach of pea plants grown in split-root-system where one half of the root was well-irrigated and the other was subjected to drought. Water stress locally provoked nodule water potential decrease that led to SNF local inhibition. The proteomic approach revealed 11 and 7 nodule proteins regulated by drought encoded by P. sativum and R. leguminosarum genomes respectively. Among these 18 proteins, three proteins related to flavonoid metabolism, two to sulphur metabolism and three RNA-binding proteins were identified. These proteins could be molecular targets for future studies focused on the improvement of legumes tolerance to drought. Moreover, this work also provides new hints for the deciphering of SNF regulation machinery in nodules.Publication Open Access Assessing the efficiency of dimethylpyrazole-based nitrification inhibitors under elevated CO2 conditions(Elsevier, 2021) Bozal-Leorri, Adrián; González Murua, Carmen; Marino Bilbao, Daniel; Aparicio Tejo, Pedro María; Corrochano Monsalve, Mario; Institute for Multidisciplinary Research in Applied Biology - IMABNitrification inhibitors (NIs) are useful tools to reduce nitrogen (N) losses derived from fertilization in agriculture. However, it remains unclear whether a future climate scenario with elevated CO2 could affect NIs efficiency. Thus, the objective of this work was to study whether the increase of atmospheric CO2 concentration would affect the efficiency of two dimethylpyrazole-based NIs: 3,4-dimethylpyrazol phosphate (DMPP) and 3,4-dimethylpyrazol succinic acid (DMPSA) in a plant-soil microcosm. To do so, Hordeum vulgare var. Henley plants were grown in soil fertilized with ammonium sulphate (AS) with or without NIs under controlled environmental conditions at ambient CO2 (aCO(2)) or elevated CO2 (eCO(2); 700 ppm). In the soil, mineral nitrogen and N2O emission evolution were monitored together with nitrifying and denitrifying population that were quantified by qPCR. In the plant, biomass, total amino acid content and isotopic discrimination of N and C were measured. Both NIs showed greater efficiency to maintain soil NH4+ content under eCO(2) compared to aCO(2), as a consequence of 80% reduction of AOB abundance in eCO(2). Indeed, both inhibitors were able to lessen 53% the N2O emissions in eCO(2) compared to aCO(2). Regarding the plant, DMPP and DMPSA negatively affected plant biomass at aCO(2) but this effect was restored at eCO(2) due to a better ammonium tolerance associated with an increase in total amino acid content. Overall, DMPP and DMPSA NIs were highly efficient under eCO(2), reducing N2O emissions and keeping N in the soil stable for longer while maintaining plant biomass production.Publication Open Access Can ammonium stress be positive for plant performance?(Frontiers Media, 2019) Marino Bilbao, Daniel; Morán Juez, José Fernando; Institute for Multidisciplinary Research in Applied Biology - IMABIn this article, we propose a change of paradigm where ammonium nutrition may be considered not exclusively as an undesirable situation for plant performance, but as a way to provoke changes in plant metabolism that can be beneficial for crop quality and plant physiology. While some of the positive effects of ammonium referred here still require further evaluation, the cross-tolerance induction of NH+4 to certain subsequent stresses, notably salinity, is clear. However, the molecular actors governing these interactions are almost completely unknown, and future works will be essential in order to fully exploit the benefits of ammonium-based fertilizers.