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Nitrogen is an essential nutrient for plant growth. World-wide, large quantities of nitrogenous fertilizer are applied to ensure maximum crop productivity. However, nitrogen fertilizer application is expensive and negatively affects the environment, and subsequently human health. A strategy to address this problem is the development of crops that are efficient in acquiring and using nitrogen and that can achieve high seed yields with reduced nitrogen input. This review integrates the current knowledge regarding inorganic and organic nitrogen management at the whole-plant level, spanning from nitrogen uptake to remobilization and utilization in source and sink organs. Plant partitioning and transient storage of inorganic and organic nitrogen forms are evaluated, as is how they affect nitrogen availability, metabolism and mobilization. Essential functions of nitrogen transporters in source and sink organs and their importance in regulating nitrogen movement in support of metabolism, and vegetative and reproductive growth are assessed. Finally, we discuss recent advances in plant engineering, demonstrating that nitrogen transporters are effective targets to improve crop productivity and nitrogen use efficiency. While inorganic and organic nitrogen transporters were examined separately in these studies, they provide valuable clues about how to successfully combine approaches for future crop engineering.

Glutamate (Glu) metabolism and amino acid translocation were investigated in the young and old leaves of tobacco (Nicotiana tabacum L. cv Xanthi) using [N-15] ammonium and [2-N-15] Glu tracers. Regardless of leaf age, [N-15] ammonium assimilation occurred via glutamine synthetase (GS;EC 6.1.1.3) and Glu synthase ( ferredoxin [Fd]-GOGAT; EC 1.4.7.1; NADH-GOGAT; EC 1.4.1.14), both in the light and darkness, and it did not depend on Glu dehydrogenase (GDH;EC 1.4.1.2). The [N-15] ammonium and ammonium accumulation patterns support the role of GDH in the deamination of [2-N-15] Glu to provide 2-oxoglutarate and [N-15] ammonium. In the dark, excess [N-15] ammonium was incorporated into asparagine that served as an additional detoxification molecule. The constant Glu levels in the phloem sap suggested that Glu was continuously synthesized and supplied into the phloem regardless of leaf age. Further study using transgenic tobacco lines, harboring the promoter of the GLU1 gene (encoding Arabidopsis [Arabidopsis thaliana] Fd-GOGAT) fused to a GUS reporter gene, revealed that the expression of Fd-GOGAT remained higher in young leaves compared to old leaves, and higher in the veins compared to the mesophyll. Confocal laser-scanning microscopy localized the Fd-GOGAT protein to the phloem companion cells-sieve element complex in the leaf veins. The results are consistent with a role of Fd-GOGAT in supplying Glu for the synthesis and transport of amino acids. Taken together, the data provide evidence that the GS-GOGAT pathway and GDH play distinct roles in the source-sink nitrogen cycle of tobacco leaves.

Autophagy is a universal mechanism in eukaryotic cells that facilitates the degradation of unwanted cell constituents and is essential for cell homeostasis and nutrient recycling.The salicylic acid‐independent effects of autophagy defects on leaf metabolism were determined through large‐scale proteomic and lipidomic analyses of atg5 and atg5/sid2 mutants under different nitrogen and sulfur growth conditions.Results revealed that irrespective of the growth conditions, plants carrying the atg5 mutation presented all the characteristics of endoplasmic reticulum (ER) stress. Increases in peroxisome and ER proteins involved in very long chain fatty acid synthesis and β‐oxidation indicated strong modifications of lipid metabolism. Lipidomic analyses revealed changes in the concentrations of sphingolipids, phospholipids and galactolipids. Significant accumulations of phospholipids and ceramides and changes in GIPCs (glycosyl‐inositol‐phosphoryl‐ceramides) in atg5 mutants indicated large modifications in endomembrane‐lipid and especially plasma membrane‐lipid composition. Decreases in chloroplast proteins and galactolipids in atg5 under low nutrient conditions, indicated that chloroplasts were used as lipid reservoirs for β‐oxidation in atg5 mutants.In conclusion, this report demonstrates the strong impact of autophagy defect on ER stress and reveals the role of autophagy in the control of plant lipid metabolism and

Autophagy is a ubiquitous vesicular process for protein and organelle recycling in eukaryotes. In plant, autophagy is reported to play pivotal roles in nutrient recycling, adaptation to biotic and abiotic stresses. The role of autophagy in plant immunity remains poorly understood. Several reports showed enhanced susceptibility of different Arabidopsis autophagy mutants ( atg ) to necrotrophic fungal pathogens. Interaction of necrotrophic bacterial pathogens with autophagy is overlooked. We then investigated such interaction by inoculating the necrotrophic enterobacterium Dickeya dadantii in leaves of the atg2 and atg5 mutants and an ATG8a overexpressing line. Overexpressing ATG8a enhances plant tolerance to D. dadantii . While atg5 mutant displayed similar susceptibility to the WT, the atg2 mutant exhibited accelerated leaf senescence and enhanced susceptibility upon infection. Both phenotypes were reversed when the sid2 mutation, abolishing SA signaling, was introduced in the atg2 mutant. High levels of SA signaling in atg2 mutant resulted in repression of the jasmonic acid (JA) defense pathway known to limit D. dadantii progression in A. thaliana . We provide evidence that in atg2 mutant, the disturbed hormonal balance leading to higher SA signaling is the main factor causing increased susceptibility to the D. dadantii necrotroph by repressing the JA pathway and accelerating developmental senescence.

Autophagy is essential for nutrient recycling and plays a fundamental role in seed production and grain filling in plants. Autophagy participates in nitrogen remobilization at the whole-plant level, and the seeds of autophagy mutants present abnormal C and N contents relative to wild-type (WT) plants. It is well known that autophagy (ATG) genes are induced in leaves during senescence; however, expression of such genes in seeds has not yet been reported. In this study we show that most of the ATG genes are induced during seed maturation in Arabidopsis siliques. Promoter-ATG8f::UIDA and promoter-ATG8f::GFP fusions showed the strong expression of ATG8f in the phloem companion cells of pericarps and the funiculus, and in the embryo. Expression was especially strong at the late stages of development. The presence of many GFP-ATG8 pre-autophagosomal structures and autophagosomes confirmed the presence of autophagic activity in WT seed embryos. Seeds of atg5 and WT plants grown under low-or high-nitrate conditions were analysed. Nitrate-independent phenotypes were found with higher seed abortion in atg5 and early browing, higher total protein concentrations in the viable seeds of this mutant as compared to the WT. The higher total protein accumulation in atg5 viable seeds was significant from early developmental stages onwards. In addition, relatively low and early accumulation of 12S globulins were found in atg5 seeds. These features led us to the conclusion that atg5 seed development is accelerated and that the protein storage deposition pathway is somehow abnormal or incomplete.

Comparison of the extent of leaf senescence depending on the genetic background of different recombinant inbred lines (RILs) of Arabidopsis (Arabidopsis thaliana) is described. Five RILs of the Bay-0 x Shahdara population showing differential leaf senescence phenotypes (from early senescing to late senescing) were selected to determine metabolic markers to discriminate Arabidopsis lines on the basis of senescence-dependent changes in metabolism. The proportion of [gamma]-aminobutyric acid, leucine, isoleucine, aspartate, and glutamate correlated with (1) the age and (2) the senescence phenotype of the RILs. Differences were observed in the glycine/serine ratio even before any senescence symptoms could be detected in the rosettes. This could be used as predictive indicator for plant senescence behavior. Surprisingly, late-senescing lines appeared to mobilize glutamine, asparagine, and sulfate more efficiently than early-senescing lines. The physiological basis of the relationship between leaf senescence and flowering time was analyzed.

Five recombinant inbred lines (RILs) of Arabidopsis (Arabidopsis thaliana), previously selected from the Bay-0X Shahdara RIL population on the basis of differential leaf senescence phenotypes ( from early senescing to late senescing) when cultivated under nitrogen ( N)- limiting conditions, were analyzed to monitor metabolic markers related to N assimilation and N remobilization pathways. In each RIL, a decrease of total N, free amino acid, and soluble protein contents with leaf aging was observed. In parallel, the expression of markers for N remobilization such as cytosolic glutamine synthetase, glutamate dehydrogenase, and CND41- like protease was increased. This increase occurred earlier and more rapidly in early-senescing lines than in late-senescing lines. We measured the partitioning of (15) N between sink and source leaves during the vegetative stage of development using (15) N tracing and showed that N remobilization from the source leaves to the sink leaves was more efficient in the early-senescing lines. The N remobilization rate was correlated with leaf senescence severity at the vegetative stage. Experiments of (15) N tracing at the reproductive stage showed, however, that the rate of N remobilization from the rosettes to the flowering organs and to the seeds was similar in early- and late-senescing lines. At the reproductive stage, N remobilization efficiency did not depend on senescence phenotypes but was related to the ratio between the biomasses of the sink and the source organs.

Protein hydrolysates have gained interest as plant biostimulants due to their positive effects on plant performances. They are mainly composed of amino acids, but there is no evidence of the role of individual of amino acids as biostimulants. In this study we carried out in vitro experiments to monitor the development of Arabidopsis seedlings on amino acid containing media in order to analyze the biostimulant properties of the twenty individual proteinogenic amino acids. We demonstrated that proteinogenic amino acids are not good nitrogen sources as compared to nitrate for plant growth. Biostimulant analyses were based on leaf area measurements as a proxy of plant growth. We developed the Amino Acid Use Efficiency index to quantify the biostimulating effect of individual amino acids in the presence of nitrate. This index allowed us to classify amino acids into three groups, characterized by their inhibiting, neutral, and beneficial effects regarding leaf area. Glutamine and asparagine demonstrated the most significant effects in promoting leaf area in the presence of nitrate supply. The stimulating effect was confirmed by using the L and D enantiomeric forms. Both L-glutamine and L-asparagine stimulated leaf area at low concentrations, emphasizing their biostimulating properties. Our plant growth design and AAUE index pave the way for the identification of other bioactive molecules in protein hydrolysates and for the comparison of biostimulant performances.

To investigate the role of stress in nitrogen management in plants, the effect of pathogen attack, elicitors, and phytohormone application on the expression of the two senescence-related markers GS1 (cytosolic glutamine synthetase EC 6.3.1.2) and GDH (glutamate dehydrogenase, EC 1.4.1.2) involved in nitrogen mobilization in senescing leaves of tobacco (Nicotiana tabacum L.) plants, was studied. The expression of genes involved in primary nitrogen assimilation such as GS2 (chloroplastic glutamine synthetase) and Nia (nitrate reductase, EC 1.6.1.1) was also analysed. The Glubas gene, coding a beta-1,3-glucanase, was used as a plant-defence gene control. As during natural senescence, the expression of GS2 and Nia was repressed under almost all stress conditions. By contrast, GS1 and GDH mRNA accumulation was increased. However, GS1 and GDH showed differential patterns of expression depending on the stress applied. The expression of GS1 appeared more selective than GDH. Results indicate that the GDH and GS1 genes involved in leaf senescence are also a component of the plant defence response during plant-pathogen interaction. The links between natural plant senescence and stress-induced senescence are discussed, as well as the potential role of GS1 and GDH in a metabolic safeguard process.

Autophagy is present at a basal level in all plant tissues and is induced during leaf ageing and in response to nitrogen (N) starvation. Nitrogen remobilization from the rosette to the seeds is impaired in autophagy mutants. This report focuses on the role of autophagy in leaf N management and proteolysis during plant ageing. Metabolites, enzyme activities and protein contents were monitored in several autophagy-defective (atg) Arabidopsis mutants grown under low and high nitrate conditions. Results showed that carbon (C) and N statuses were affected in atg mutants before any senescence symptoms appeared. atg mutants accumulated larger amounts of ammonium, amino acids and proteins than wild type, and were depleted in sugars. Over-accumulation of proteins in atg mutants was selective and occurred despite higher endopeptidase and carboxypeptidase activities. Specific over-accumulation of the ribosomal proteins S6 and L13 subunits, and of catalase and glutamate dehydrogenase proteins was observed. atg mutants also accumulated peptides putatively identified as degradation products of the Rubisco large subunit and glutamine synthetase 2 (GS2). Incomplete chloroplast protein degradation resulting from autophagy defects could explain the higher N concentrations measured in atg rosettes and defects in N remobilization. It is concluded that autophagy controls C : N status and protein content in leaves of Arabidopsis.