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Plant Nitrogen Assimilation and Metabolism

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A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 49816

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Prof. Dr. Concepción Avila

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Guest Editor

Molecular Biology and Biochemistry Department, Málaga University, E-29071 Málaga, Spain
Interests: plant nitrogen metabolism; transcriptional regulation in trees; conifer genomics; evolution

Prof. Dr. Fernando de la Torre

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Guest Editor

Molecular Biology and Biochemistry Department Málaga University, E-29071 Málaga, Spain
Interests: plant nitrogen metabolism; biosynthesis of phenolic compounds; transcriptional and biochemical regulation of plant metabolism; chloroplast biochemistry; evolution of amino acid biosynthetic pathways

Special Issue Information

Dear Colleagues,

Nitrogen is an essential element for plant growth and animal nutrition, and is a nutrient that is taken up in a large amount by plants. Limitations in food supply for a growing population, together with the harmful effects of intensive agriculture on the environment, are major challenges to agricultural science. The development of crop plants with improved nitrogen assimilation and management would reduce the need for intensive nitrogen fertilization, and positively influence the environment. Major efforts have been carried out over the last century in order to understand the biochemistry and molecular biology of nitrogen metabolism in plants, and to design how this knowledge may be applied in order to improve crops. In addition, the new high-throughput technologies in biology, along with systems biology approaches, may provide new integrated information about the processes determinants of nitrogen use efficiency (NUE) in plants, and the discovery of new genes involved in the underlying molecular mechanisms. This knowledge could allow for the design of new biotechnological approaches to improve nitrogen management by crop plants, and contribute to developing models of sustainable agriculture with a lower environmental impact. This Special Issue intends to bring together the state-of-the-art in nitrogen metabolism of plants and model microorganisms.

Prof. Dr. Concepción Avila
Prof. Dr. Fernando de la Torre
Guest Editors

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Keywords

allocation and mobilization
assimilation
biotechnological and agronomical approaches, high-throughput technologies for nitrogen management
nitrogen metabolism
nitrogen use efficiency, regulation, transport

Published Papers (12 papers)

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Editorial

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4 pages, 222 KiB

Open AccessEditorial

Special Issue Editorial: Plant Nitrogen Assimilation and Metabolism

by Fernando de la Torre and Concepción Ávila

Plants 2021, 10(7), 1278; https://0-doi-org.brum.beds.ac.uk/10.3390/plants10071278 - 23 Jun 2021

Cited by 3 | Viewed by 2099

Abstract

Nitrogen is an important macronutrient for plant growth and development. Research has long been carried out to elucidate the mechanisms involved in nitrogen uptake, assimilation, and utilization in plants. However, despite recent advances, many of these mechanisms still are not fully understood. In this special issue, several research articles and two reviews, all of them aiming to elucidate some specific aspects of nitrogen (N) metabolism, are presented. Together, the articles in this issue provide a state-of-the-art perspective on important questions related to nitrogen metabolism in photosynthetic organisms, highlighting the fundamental importance of research in this field. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

Research

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16 pages, 7329 KiB

Open AccessFeature PaperArticle

Drought-Induced Responses of Nitrogen Metabolism in Ipomoea batatas

by Houqiang Xia, Tao Xu, Jing Zhang, Ke Shen, Zongyun Li and Jingran Liu

Plants 2020, 9(10), 1341; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9101341 - 11 Oct 2020

Cited by 27 | Viewed by 2728

Abstract

This study investigated the effect of water stress, simulated by the polyethylene glycol (PEG-6000) method, on nitrogen (N) metabolism in leaves and roots of hydroponically grown sweet potato seedlings, Xushu 32 (X32) and Ningzishu 1 (N1). The concentrations of PEG-6000 treatments were 0%, 5% and 10% (m/v). The results showed that the drought-treated plants showed a decline leaf relative water content, and revealed severe growth inhibition, compared with the 0% treatment. Under drought stress, the decline in biomass of the leaf and stem was more noticeable than in root biomass for X32, leading to a higher root to shoot ratio. Drought stress increased the nitrate nitrogen (NO₃⁻-N) and protein in leaves, but reduced all the activities of N-metabolism enzymes and the transcriptional levels of nitrate reductase (NR), glutamine synthetase (GS) and glutamate synthase (GOGAT); in roots, NO₃⁻-N and NR had opposite trends. The leaf ammonium nitrogen (NH₄⁺-N), GS and amino acid had different trends between X32 and N1 under drought stress. Furthermore, the transcriptional level of nitrate transporter genes NRT1.1 in leaves and roots were upregulated under drought stress, except in N1 roots. In conclusion, NR determined the different response to drought in leaves for X32 and N1, and GS and GOGAT determined the response to drought in roots, respectively. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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17 pages, 2715 KiB

Open AccessArticle

Enzymes Involved in the Biosynthesis of Arginine from Ornithine in Maritime Pine (Pinus pinaster Ait.)

by José Alberto Urbano-Gámez, Jorge El-Azaz, Concepción Ávila, Fernando N. de la Torre and Francisco M. Cánovas

Plants 2020, 9(10), 1271; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9101271 - 27 Sep 2020

Cited by 12 | Viewed by 4002

Abstract

The amino acids arginine and ornithine are the precursors of a wide range of nitrogenous compounds in all living organisms. The metabolic conversion of ornithine into arginine is catalyzed by the sequential activities of the enzymes ornithine transcarbamylase (OTC), argininosuccinate synthetase (ASSY) and argininosuccinate lyase (ASL). Because of their roles in the urea cycle, these enzymes have been purified and extensively studied in a variety of animal models. However, the available information about their molecular characteristics, kinetic and regulatory properties is relatively limited in plants. In conifers, arginine plays a crucial role as a main constituent of N-rich storage proteins in seeds and serves as the main source of nitrogen for the germinating embryo. In this work, recombinant PpOTC, PpASSY and PpASL enzymes from maritime pine (Pinus pinaster Ait.) were produced in Escherichia coli to enable study of their molecular and kinetics properties. The results reported here provide a molecular basis for the regulation of arginine and ornithine metabolism at the enzymatic level, suggesting that the reaction catalyzed by OTC is a regulatory target in the homeostasis of ornithine pools that can be either used for the biosynthesis of arginine in plastids or other nitrogenous compounds in the cytosol. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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11 pages, 290 KiB

Open AccessCommunication

Corn Responsiveness to Azospirillum: Accessing the Effect of Root Exudates on the Bacterial Growth and Its Ability to Fix Nitrogen

by Lucas Caiubi Pereira, Carolina Bertuzzi Pereira, Larissa Vinis Correia, Thaisa Cavalieri Matera, Rayssa Fernanda dos Santos, Cristiane de Carvalho, Elisete Aparecida Fernandes Osipi and Alessandro Lucca Braccini

Plants 2020, 9(7), 923; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9070923 - 21 Jul 2020

Cited by 10 | Viewed by 2666

Abstract

Corn has shown different degrees of positive response to inoculation with the nitrogen- fixing bacteria of the genera Azospirillum. Part of it has been attributed to the plant genotypic variation, including the root exudates, that are used by the bacteria as energy source. In this study, we grew two corn hybrids that differ for their response to Azospirillum, to investigate the effect of different exudates profiles on the bacteria growth and nitrogenase activity. Employing high performance liquid chromatography, we identified nine amino acids (asparagine, aspartic acid, serine, glutamic acid, valine, phenylalanine, threonine, tryptophan and alanine), six sugars (glucose, sucrose, xylose, arabinose, fructose and galactose) and four organic acids (citrate, malate, succinate and fumarate). The less responsive corn genotype showed reduced plant growth (root volume, shoot dry mass and shoot N content), a lower concentration of Azospirillum cells within the root tissues, a higher content of asparagine and glucose and a reduced amount of metabolites that serve as bacterial energy source (all organic acids + five sugars, excluding glucose). The genotypes did not interfere in the ability of Azospirillum to colonize the substrate, but the metabolites released by the less responsive one reduced the nitrogenase activity. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

14 pages, 2234 KiB

Open AccessArticle

Exogenous Carbon Compounds Modulate Tomato Root Development

by Ana Isabel González-Hernández, Loredana Scalschi, Pilar García-Agustín and Gemma Camañes

Plants 2020, 9(7), 837; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9070837 - 03 Jul 2020

Cited by 6 | Viewed by 2489

Abstract

NO₃⁻ is not only a nutrient, but also a signaling compound that plays an important role in several plant processes, like root development. The present study aimed to investigate the effect of three different exogenous C compounds (sucrose, glucose, 2-oxoglutarate) added to NO₃⁻ nutrition on C/N, auxin and antioxidant metabolisms in 10-day-old tomato seedlings. Sucrose and glucose supplementation enhanced primary root (PR) length, lateral root number and root density, while 2-oxoglutarate negatively affected them. This phenomenon was accompanied by a slight increase in NRT2.1 and GS1 gene expression, together with an increase in LAX2 and LAX3 and a decrease in LAX4 in the roots growing under sucrose and glucose sources. The addition of 2-oxoglutarate enhanced the expression of NiR, GDH, PEPC1, LAX1, LAX3 and the antioxidant gene SOD Cl. Taken together, these findings contribute to a better understanding of how these C sources can modulate N uptake and C/N, auxin and antioxidant gene expression, which could be useful for improving nitrogen use efficiency. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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19 pages, 2232 KiB

Open AccessArticle

Inorganic Nitrogen Form Determines Nutrient Allocation and Metabolic Responses in Maritime Pine Seedlings

by Francisco Ortigosa, José Miguel Valderrama-Martín, José Alberto Urbano-Gámez, María Luisa García-Martín, Concepción Ávila, Francisco M. Cánovas and Rafael A. Cañas

Plants 2020, 9(4), 481; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9040481 - 09 Apr 2020

Cited by 6 | Viewed by 3782

Abstract

Nitrate and ammonium are the main forms of inorganic nitrogen available to plants. The present study aimed to investigate the metabolic changes caused by ammonium and nitrate nutrition in maritime pine (Pinus pinaster Ait.). Seedlings were grown with five solutions containing different proportions of nitrate and ammonium. Their nitrogen status was characterized through analyses of their biomass, different biochemical and molecular markers as well as a metabolite profile using ¹H-NMR. Ammonium-fed seedlings exhibited higher biomass than nitrate-fed-seedlings. Nitrate mainly accumulated in the stem and ammonium in the roots. Needles of ammonium-fed seedlings had higher nitrogen and amino acid contents but lower levels of enzyme activities related to nitrogen metabolism. Higher amounts of soluble sugars and L-arginine were found in the roots of ammonium-fed seedlings. In contrast, L-asparagine accumulated in the roots of nitrate-fed seedlings. The differences in the allocation of nitrate and ammonium may function as metabolic buffers to prevent interference with the metabolism of photosynthetic organs. The metabolite profiles observed in the roots suggest problems with carbon and nitrogen assimilation in nitrate-supplied seedlings. Taken together, this new knowledge contributes not only to a better understanding of nitrogen metabolism but also to improving aspects of applied mineral nutrition for conifers. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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18 pages, 1740 KiB

Open AccessEditor’s ChoiceArticle

Nitrogen Assimilation in the Highly Salt- and Boron-Tolerant Ecotype Zea mays L. Amylacea

by Teresa Fuertes-Mendizábal, Elizabeth Irica Bastías, Carmen González-Murua and Mª Begoña González-Moro

Plants 2020, 9(3), 322; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9030322 - 04 Mar 2020

Cited by 19 | Viewed by 7883

Abstract

The Lluta Valley in Northern Chile is an important agricultural area affected by both salinity and boron (B) toxicity. Zea mays L. amylacea, an ecotype arisen because of the seed selection practiced in this valley, shows a high tolerance to salt and B levels. In the present study the interaction between B and salt was studied after 20 days of treatment at low (100 mM) and high salinity (430 mM NaCl), assessing changes in nitrogen metabolites and in the activity of key nitrogen-assimilating enzymes. Under non-saline conditions, the presence of excessive B favored higher nitrate and ammonium mobilization to leaves, increasing nitrate reductase (NR) activity but not glutamine synthetase (GS). Thus, the increment of nitrogen use efficiency by B application would contribute partially to maintain the biomass production in this ecotype. Positive relationships between NR activity, nitrate, and stomatal conductance were observed in leaves. The increment of major amino acids alanine and serine would indicate a photoprotective role of photorespiration under low-salinity conditions, thus the inhibition of nitrogen assimilation pathway (NR and GS activities) occurred only at high salinity. The role of cytosolic GS regarding the proline accumulation is discussed. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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18 pages, 2796 KiB

Open AccessArticle

Variations in Nitrogen Metabolism are Closely Linked with Nitrogen Uptake and Utilization Efficiency in Cotton Genotypes under Various Nitrogen Supplies

by Asif Iqbal, Qiang Dong, Xiangru Wang, Huiping Gui, Hengheng Zhang, Xiling Zhang and Meizhen Song

Plants 2020, 9(2), 250; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9020250 - 15 Feb 2020

Cited by 30 | Viewed by 3136

Abstract

Cotton production is highly sensitive to nitrogen (N) fertilization, whose excessive use is responsible for human and environmental problems. Lowering N supply together with the selection of N-efficient genotypes, more able to uptake, utilize, and remobilize the available N, could be a challenge to maintain high cotton production sustainably. The current study aimed to explore the intraspecific variation among four cotton genotypes in response to various N supplies, in order to identify the most distinct N-efficient genotypes and their nitrogen use efficiency (NUE)-related traits in hydroponic culture. On the basis of shoot dry matter, CCRI-69 and XLZ-30 were identified as N-efficient and N-inefficient genotypes, respectively, and these results were confirmed by their contrasting N metabolism, uptake (NUpE), and utilization efficiency (NUtE). Overall, our results indicated the key role of shoot glutamine synthetase (GS) and root total soluble protein in NUtE. Conversely, tissue N concentration and N-metabolizing enzymes were considered as the key traits in conferring high NUpE. The remobilization of N from the shoot to roots by high shoot GS activity may be a strategy to enhance root total soluble protein, which improves root growth for N uptake and NUE. In future, multi-omics studies will be employed to focus on the key genes and pathways involved in N metabolism and their role in improving NUE. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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18 pages, 1929 KiB

Open AccessArticle

NADH-GOGAT Overexpression Does Not Improve Maize (Zea mays L.) Performance Even When Pyramiding with NAD-IDH, GDH and GS

by Rafael A. Cañas, Zhazira Yesbergenova-Cuny, Léo Belanger, Jacques Rouster, Lenaïg Brulé, Françoise Gilard, Isabelle Quilleré, Christophe Sallaud and Bertrand Hirel

Plants 2020, 9(2), 130; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9020130 - 21 Jan 2020

Cited by 26 | Viewed by 4585

Abstract

Maize plants overexpressing NADH-GOGAT were produced in order to determine if boosting 2-Oxoglurate production used as a carbon skeleton for the biosynthesis of amino acids will improve plant biomass and kernel production. The NADH-GOGAT enzyme recycles glutamate and incorporates carbon skeletons into the ammonium assimilation pathway using the organic acid 2-Oxoglutarate as a substrate. Gene pyramiding was then conducted with NAD-IDH and NADH-GDH, two enzymes also involved in the synthesis of 2-Oxoglurate. NADH-GOGAT overexpression was detrimental for shoot biomass production but did not markedly affect kernel yield. Additional NAD-IDH and NADH-GDH activity did not improve plant performance. A decrease in kernel production was observed when NADH-GDH was pyramided to NADH-GOGAT and NAD-IDH. This decrease could not be restored even when additional cytosolic GS activity was present in the plants overexpressing the three enzymes producing 2-Oxoglutarate. Detailed leaf metabolic profiling of the different transgenic plants revealed that the NADH-GOGAT over-expressors were characterized by an accumulation of amino acids derived from glutamate and a decrease in the amount of carbohydrates further used to provide carbon skeletons for its synthesis. The study suggests that 2-Oxoglutarate synthesis is a key element acting at the interface of carbohydrate and amino acid metabolism and that its accumulation induces an imbalance of primary carbon and nitrogen metabolism that is detrimental for maize productivity. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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15 pages, 2953 KiB

Open AccessArticle

Dynamics of Short-Term Metabolic Profiling in Radish Sprouts (Raphanus sativus L.) in Response to Nitrogen Deficiency

by Seung-A Baek, Kyung-Hoan Im, Sang Un Park, Sung-Dug Oh, Jaehyuk Choi and Jae Kwang Kim

Plants 2019, 8(10), 361; https://0-doi-org.brum.beds.ac.uk/10.3390/plants8100361 - 23 Sep 2019

Cited by 9 | Viewed by 2753

Abstract

Nitrogen (N) is a macronutrient important for the survival of plants. To investigate the effects of N deficiency, a time-course metabolic profiling of radish sprouts was performed. A total of 81 metabolites—including organic acids, inorganic acid, amino acids, sugars, sugar alcohols, amines, amide, sugar phosphates, policosanols, tocopherols, phytosterols, carotenoids, chlorophylls, and glucosinolates—were characterized. Principal component analysis and heat map showed distinction between samples grown under different N conditions, as well as with time. Using PathVisio, metabolic shift in biosynthetic pathways was visualized using the metabolite data obtained for 7 days. The amino acids associated with glucosinolates accumulated as an immediate response against –N condition. The synthesis of pigments and glucosinolates was decreased, but monosaccharides and γ-tocopherol were increased as antioxidants in radish sprouts grown in –N condition. These results indicate that in radish sprouts, response to N deficiency occurred quickly and dynamically. Thus, this metabolic phenotype reveals that radish responds quickly to N deficiency by increasing the content of soluble sugars and γ-tocopherol, which acts as a defense mechanism after the germination of radish seeds. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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Review

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14 pages, 735 KiB

Open AccessReview

Chlamydomonas reinhardtii, an Algal Model in the Nitrogen Cycle

by Carmen M. Bellido-Pedraza, Victoria Calatrava, Emanuel Sanz-Luque, Manuel Tejada-Jiménez, Ángel Llamas, Maxence Plouviez, Benoit Guieysse, Emilio Fernández and Aurora Galván

Plants 2020, 9(7), 903; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9070903 - 16 Jul 2020

Cited by 22 | Viewed by 7026

Abstract

Nitrogen (N) is an essential constituent of all living organisms and the main limiting macronutrient. Even when dinitrogen gas is the most abundant form of N, it can only be used by fixing bacteria but is inaccessible to most organisms, algae among them. Algae preferentially use ammonium (NH₄⁺) and nitrate (NO₃⁻) for growth, and the reactions for their conversion into amino acids (N assimilation) constitute an important part of the nitrogen cycle by primary producers. Recently, it was claimed that algae are also involved in denitrification, because of the production of nitric oxide (NO), a signal molecule, which is also a substrate of NO reductases to produce nitrous oxide (N₂O), a potent greenhouse gas. This review is focused on the microalga Chlamydomonas reinhardtii as an algal model and its participation in different reactions of the N cycle. Emphasis will be paid to new actors, such as putative genes involved in NO and N₂O production and their occurrence in other algae genomes. Furthermore, algae/bacteria mutualism will be considered in terms of expanding the N cycle to ammonification and N fixation, which are based on the exchange of carbon and nitrogen between the two organisms. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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22 pages, 1532 KiB

Open AccessReview

Flavonoids and Isoflavonoids Biosynthesis in the Model Legume Lotus japonicus; Connections to Nitrogen Metabolism and Photorespiration

by Margarita García-Calderón, Carmen M. Pérez-Delgado, Peter Palove-Balang, Marco Betti and Antonio J. Márquez

Plants 2020, 9(6), 774; https://0-doi-org.brum.beds.ac.uk/10.3390/plants9060774 - 20 Jun 2020

Cited by 43 | Viewed by 5113

Abstract

Phenylpropanoid metabolism represents an important metabolic pathway from which originates a wide number of secondary metabolites derived from phenylalanine or tyrosine, such as flavonoids and isoflavonoids, crucial molecules in plants implicated in a large number of biological processes. Therefore, various types of interconnection exist between different aspects of nitrogen metabolism and the biosynthesis of these compounds. For legumes, flavonoids and isoflavonoids are postulated to play pivotal roles in adaptation to their biological environments, both as defensive compounds (phytoalexins) and as chemical signals in symbiotic nitrogen fixation with rhizobia. In this paper, we summarize the recent progress made in the characterization of flavonoid and isoflavonoid biosynthetic pathways in the model legume Lotus japonicus (Regel) Larsen under different abiotic stress situations, such as drought, the impairment of photorespiration and UV-B irradiation. Emphasis is placed on results obtained using photorespiratory mutants deficient in glutamine synthetase. The results provide different types of evidence showing that an enhancement of isoflavonoid compared to standard flavonol metabolism frequently occurs in Lotus under abiotic stress conditions. The advance produced in the analysis of isoflavonoid regulatory proteins by the use of co-expression networks, particularly MYB transcription factors, is also described. The results obtained in Lotus japonicus plants can be also extrapolated to other cultivated legume species, such as soybean, of extraordinary agronomic importance with a high impact in feeding, oil production and human health. Full article

(This article belongs to the Special Issue Plant Nitrogen Assimilation and Metabolism)

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