JXB Advance Access originally published online on December 18, 2007
Journal of Experimental Botany 2008 59(1):111-119; doi:10.1093/jxb/erm208
SPECIAL ISSUE REVIEW PAPER |
Amino acids and nitrate as signals for the regulation of nitrogen acquisition
1Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK
2College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, PR China
* To whom correspondence should be addressed. E-mail: tony.miller{at}bbsrc.ac.uk
Received 29 March 2007; Revised 9 August 2007 Accepted 9 August 2007
 |
Abstract |
|---|
 Top Abstract IntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
The uptake of nitrogen (N) by roots is known to change with supply in a manner that suggests that the N status of plants is somehow sensed and can feedback to regulate this process. The most abundant source of N in soils for crops is nitrate. Uptake systems for nitrate, ammonium, and amino acids are present in the roots of most plants including crops. As nitrate is assimilated via conversion to nitrite, then ammonium into amino acids, it has been suggested that the internal pools of amino acids within plants may indicate nitrogen status by providing a signal that can regulate nitrate uptake by the plant. In support of this idea, both nitrate and ammonium influx and transporter transcript were shown to decrease in root tissue treated with exogenously applied amino acids. Several different amino acids have been tested for their effects on influx and transcription and glutamine was most effective. The feedback regulation occurs by changing the expression of transporters, but may also involve the post-translational modification of proteins. For example, some of the cytoplasmic enzymes responsible for nitrate assimilation are regulated by phosphorylation and binding of a 14-3-3 protein. The effects of treating plants with glutamine have been examined, first to identify the uptake of the amino acid and then to measure tissue nitrate reductase activity and cellular pools of nitrate. These results are reviewed in terms of feedback regulation and the putative cell sensing systems for N status including a possible specific role for cytosolic nitrate.
Key words: Amino acids, ammonium uptake, feedback regulation, nitrate uptake, nitrogen sensor
|
Introduction |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
It is difficult to find any environment in which nitrogen (N) supply is not a limiting factor for plant growth; this is demonstrated by the fact that the addition of this fertilizer will stimulate the growth of any plant. Soil N is available to plants chiefly as either nitrate (NO
) or ammonium (NH
) and to a lesser extent, amino acids. Nitrogen is a fundamental regulator of plant growth and its supply can so strongly influence plant growth that it once led to the suggestion that NO was a plant hormone (Trewavas, 1983). The way in which the N status of a plant is sensed is of fundamental importance to agriculture as understanding this mechanism is key to attempts to improve N use efficiency (NUE) by crops. The imbalance between demand and supply for N in crops can result in either sub-optimal yield or the addition of environmentally damaging excesses of fertilizer. The uptake and assimilation of N by roots is known to change with supply in a manner that suggests that the N status of plants is somehow sensed and can feedback to regulate these processes. As NO is assimilated via conversion to nitrite, NH and then into amino acids, it was suggested that the internal pools of downstream N metabolites such as amino acids within plants may indicate N status by providing a signal that can regulate N uptake and assimilation by the plant (Lee and Rudge, 1986; Cooper and Clarkson, 1989).
When whole plant tissues or organs are chemically analysed these measurements show that the N status of a plant is reflected by changes in tissue pools of nitrogenous compounds, including amino acids, NO and proteins. Many different nitrogen-containing ions and molecules may be signals for N status and could be species specific, but a few favourites have emerged. For example, tissue NO testing is widely used by farmers as an indicator for crop fertilizer requirements (Westcott et al., 1993) and NO has been proposed as a biochemical signal to regulate growth, including lateral roots and shoot:root ratios (Stitt, 1999; Forde, 2002; Schieble et al., 2004). Although, it was recently argued that total shoot protein may actually be a better indicator for shoot:root ratios (Andrews et al., 2006). Laboratory experiments to test feedback regulation have treated plants directly with amino acids and the concentrations applied exogenously to roots are much higher (mM range) than those occurring in the soil (Jones et al., 2002). These high concentrations are used with the specific aim of altering the cellular pools of amino acids but it should be checked that changes in tissue concentrations can actually be measured. Another experimental approach taken has been to use chemical inhibitors to try to block specific steps in the N assimilation pathway. For example, the conversion of NH to glutamine (Gln) by glutamine synthetase (GS) can be inhibited by methionine sulphoximine (Rawat et al., 1999). In an untreated plant the source for amino acid feedback is likely to reside in the phloem (Gessler et al., 1998).
There are some general physiological effects of increasing NO supply, for example, it can provide an osmoticum, filling vacuoles and driving growth (McIntyre, 1997). Furthermore, changes in supply to the roots may also influence the long-distance flow in the xylem and this effect could result in stimulated transport of plant hormones between the root and shoot. The negative feedback model has become generally accepted by plant biologists, yet the precise nature or mechanism of the signal is not known. Even the exact location of the feedback pool within the plant is not certain, it may be the phloem sap (Gessler et al., 1998; Pal'ove-Balang and Mistrik, 2002), the apoplast or within a subcellular compartment. The link between the changes in plant N status and the molecular sensing mechanisms are difficult to integrate because studying these processes at the cellular level is problematic. These feedback effects on the uptake of each of the three main soil available N forms will be described first and then some possible molecular N sensors, followed by a consideration of the central role of amino acids and NO in this signalling process.
|
Nitrate uptake by roots |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
Plant root uptake of NO
can be negatively influenced by the external supply of amino acids or tissue concentrations of amino acids (Lee et al., 1992; Muller et al., 1995). It is a general feature of many different types of plants, including trees (Dluzniewska et al., 2006) and cell cultures (Padgett and Leonard, 1993), that supplying amino acids to roots inhibits NO uptake. The expression of inducible high affinity NO transporters can be effectively inhibited by Gln (Quesada et al., 1997; Krapp et al., 1998; Vidmar et al., 2000). Both NO-induced influx and transporter transcript abundance were decreased simultaneously in root tissue treated with exogenously applied amino acids (Vidmar et al., 2000). As amino acids can be inter-converted within plant tissues, chemical inhibitors of the conversion steps were used to identify Gln, rather than glutamate, as being responsible for down-regulating NO transporter expression (Vidmar et al., 2000). In Brassica napus, a negative correlation was found between either shoot N or NO contents and NO uptake rates, but pools of free amino acids in roots did not seem to be involved in the control of root NO uptake (Lainé et al., 1995). More recently for this species, a positive correlation between 
-aminobutyric acid in the phloem and NO uptake was reported (Beuve et al., 2004). This result is unusual because a negative feedback system is more common for most plants, although even in Brassica napus treating the roots with amino acids (Gln, glutamate, and asparagine) decreased NO uptake and transporter expression (Beuve et al., 2004).
Root NO uptake systems can be divided into transport systems that operate over different physiological ranges (Crawford and Glass, 1998) and feedback regulation by Gln on these uptake systems appears to be different. For example, Lolium perenne plants grown in sterile culture and treated for 24 h with Gln showed decreased activity of the high, but not low affinity NO uptake system (Thornton, 2004). There are several different routes whereby NO uptake can be decreased and these include both changes in gene expression and post-translational mechanisms (see review by Miller et al., 2007).
Nitrate uptake can also be influenced by NH supply and, when a mixed N source is supplied to plants, NO uptake is usually decreased (Kronzucker et al., 1999). Like amino acids, NH requires less energy input by the plant because the N is already in a reduced form by-passing this step in assimilation. However, in contrast to amino acids there can be some problems for cellular pH regulation associated with NH as an N source for the plant (Raven and Smith, 1976) and, at high external concentrations, the energy expended in effluxing this cell toxic ion (Britto et al., 2001).
|
Ammonium uptake by roots |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
The uptake of NH
by plant roots can be decreased by the external supply of amino acids and NO (Lee et al., 1992; Rawat et al., 1999). In most agricultural soils plant roots are usually exposed to more NO than NH (Miller et al., 2007). Ammonium uptake is mainly mediated by the AMT family of transporters and the regulation of this transport can occur by several different mechanisms. As this topic has been carefully reviewed in detail recently (Loqué and von Wirén, 2004), only a brief overview of some points that are relevant to transport and N status will be given here. Feeding roots with Gln and the use of a GS inhibitor has led to a model proposing that Gln in the cell altered transcription while cytosolic concentrations of NH may post-translationally regulate one AMT gene (Rawat et al., 1999). More generally, regulation of uptake can occur at the mRNA level and AMT transcripts are strongly dependent on the N status of the plant, but in Arabidopsis the pattern is different for family members. Some AMTs increase expression earlier during N deficiency while others can increase after more prolonged starvation (Loqué and von Wirén, 2004). Split-root experiments have suggested that the local root, rather than whole plant, N status regulates the expression of an NH transporter (Gansel et al., 2001). This result was different for a NO transporter where the N status of the whole plant was important (Gansel et al., 2001).
Tobacco plants with 35S-driven expression of an Arabidopsis AMT showed a 30% increase in root uptake of NH in hydroponics relative to wild-type plants (Yuan et al., 2007). However on soil supplemented with NH as an N source; these plants showed neither growth nor N acquisition differences from wild-type plants (Yuan et al., 2007). Despite expression being driven by the 35S promoter in these tobacco plants the steady-state transcripts for AtAMT1;1 were not constitutive, changing with N status of the plants and decreasing after NO or NH addition to N-deficient roots. This result suggests that the N status of a plant may directly influence mRNA turnover in plants and this may provide another regulatory mechanism for NH uptake. This result seems to contrast with that for NO transporter transcripts. In Nicotiana plumbaginifolia the expression of NpNRT2.1 driven by rolD or the 35S promoters was still high, even after treatment with 10 mM NO, when the WT endogenous gene was repressed (Fraisier et al., 2000). Post-translational regulation of AtAMT1;1 has been shown to occur via the cytosolic C terminus of the protein that results in an alteration of the interaction between the monomer components necessary for transport (Loqué et al., 2007). This mechanism provides a rapid way of regulating NH transport activity that can be linked to N supply by the phosphorylation of the C terminus.
|
Amino acid uptake by roots |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
One underlying assumption for the experiments describing the effects of externally supplied amino acids on uptake of NO
and NH is that these reduced N forms are readily taken up by roots and can directly influence the internal pools of these molecules. Uptake of radiolabelled amino acids by roots has been shown to occur (Watson and Fowden, 1975; Soldal and Nissen, 1978) and this treatment has been shown to increase some tissue pools of amino acids (Lee et al., 1992; Vidmar et al., 2000; Thornton, 2004; Fan et al., 2006). In some environments, such as arctic grassland and salt marsh, soil available amino acids are important sources of N (Henry and Jefferies, 2003; Xu et al., 2006), but in most agricultural situations the importance of this form of N has yet to be demonstrated (Jones et al., 2005). Wild plant roots can acquire soil N through fungi as mycorrhiza (Hodge, 2003) and amino acid transport can be enhanced by this relationship (Sokolovski et al., 2002), but little is known about the regulation of this uptake making it worthy of further investigation. As the activity of plasma membrane transporters in individual cells can be detected by electrophysiological measurements (Miller et al., 2001) this method has been used to assay for amino acid transport activity in coleoptiles (Kinraide et al., 1984) and roots (Fan et al., 2006). For coleoptiles the shape and duration of the change in membrane potential depended on the net charge of the amino acid (Kinraide et al., 1984). Treating barley roots with Gln gave a change in membrane potential that depended on the concentration applied and could be repeated over several cycles (Fan et al., 2006). However, repeated applications of the amino acid eventually elicited a smaller response perhaps suggesting that the transport system was sensitive to the N status of the cell. The measured affinity of this transport system for Gln was not very high (Km=1.2 mM) when compared with the likely availability of this amino acid in the soil (Jones et al., 2002). To test for root amino acid transporters with a possible role in acquisition from the soil, barley seedlings, grown in the same way as described previously in a full nutrient solution containing 10 mM nitrate (Fan et al., 2006), have been treated with 50 µM lysine. Lysine was tested because uptake of this amino acid by barley roots has been reported (Soldal and Nissen, 1978) and in the root epidermis of Arabidopsis the gene encoding the transporter has been identified (Hirner et al., 2006). Epidermal root cells treated with 50 µM lysine usually elicited a significant electrical depolarization (Fig. 1A, B, C), and the shape of the response was similar when reported from either the cytoplasm (Fig. 1A) or vacuole (Fig. 1B). The lysine treatment caused the membrane potential to become less negative (depolarization) and this effect was reversible when the amino acid was removed from the bathing solution (Fig. 1A, B). As parallel membrane potential changes were recorded from both the cytoplasm and the vacuole, this result suggests that the plasma membrane is the source of the electrical event (Miller et al., 2001). Similar electrical responses to lysine could also be obtained from barley cortical root cells (data not shown). This result might suggest that the source of the electrical response was a proton:lysine cotransporter activity at the plasma membrane (Fig. 1A). There is some evidence for a small acidification after the cell was treated with lysine (Fig. 1A), but this was not observed in all recordings and we cannot explain why this happens when the amino acid supply was removed. However, the time after the first duration of lysine exposure did not appear to significantly alter the magnitude of the transport activity (Fig. 1C). This result shows that the roots of barley seedlings have high affinity amino acid transporters that are able to access soil available N pools and the activity of this uptake system may not depend on the lysine content of the cell or perhaps the plant N status. However, more experiments are needed including molecular studies to check how the activity and expression of this transporter may change with N supply. This lysine transport activity may be analogous to that reported for LHT1 in the Arabidopsis root epidermis and has been identified as a possible target for improving NUE in crops (Hirner et al., 2006). The high affinity of this uptake system is likely to be effective in competing with rhizosphere bacteria for any available lysine.
|
The affinity of the amino acid transport system may directly depend on the N status of the plant or this may not be the only substrate for this transporter; for example, it may be a NO
transporter (Zhou et al., 1998). Clearly the N status of a plant is reflected by changes in tissue pools of nitrogenous compounds. The concentrations of some of these N-containing chemicals in tissues and sap are useful indicators of the N nutritional state of a plant. The missing link between the changes in plant experiments measuring feedback regulation of N uptake are the molecular and cellular mechanisms for the sensing of these changes in plant N status and it is this aspect that will now be reviewed.
|
Molecular nitrogen sensing systems |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
Several possible N-sensing systems have been identified that may function through sensing specific amino acids within the plant. Each one of these sensors could be the topic of a review, but for brevity we will only focus on a few key facts for each system.
PII protein
In bacteria, cellular Gln concentrations signal N status through the PII protein and a similar model has been proposed for plants (Moorhead and Smith, 2003). The PII protein is believed to sense both carbon and nitrogen status in bacteria and has been shown to directly regulate the activity of an NH transporter (Coutts et al., 2002). There are three major groups of these proteins and these have been described in detail for microbes (see review by Arcondéguy et al., 2001). Glutamine and 2-oxoglutarate concentrations in bacteria modify phosphorylation status of the PII protein which can then interact with other regulatory elements controlling the expression and activity of enzymes involved in either C or N metabolism. In cyanobacteria, 2-oxoglutarate and inorganic N sources, such as NO and NH, rather than Gln are reckoned to alter the phosphorylation status of PII (see Kobayashi et al. 2005, and references therein). Plant PII homologues have been identified in plants and evidence of a direct interaction between 2-oxoglutarate has been shown (Smith et al., 2003). A protein–protein interaction has been demonstrated between PII-like proteins and secondary components, such as kinases, providing evidence for a similar system in higher plants (Sugiyama et al., 2004). Direct proof of PII as an N sensor in plants remains elusive, although the overexpression of PII in Arabidopsis does impair the ability of plants to sense Gln (Hsieh et al., 1998), knock-out mutants show a phenotype with nitrite or ammonium as an N source (Ferrario-Méry et al., 2005, 2006). A decreased accumulation of ornithine, citrulline, and arginine led to the suggestion that PII interacts directly with N-acetyl glutamate kinase, a key enzyme in arginine biosynthesis (Ferrario-Méry et al., 2006).
Glutamate receptors
Three types of glutamate receptors are known in animals as being important for nerve transmission of signals and, in particular, at the synapse and related genes have been identified in plants (Lam et al., 1998) and Arabidopsis has a family of 20 members (Chiu et al., 2002). These plant proteins can function as calcium channels; they can be opened by both glutamate and glycine and the interaction can be synergistic (Dennison and Spalding, 2000; Dubos et al., 2003). Constitutive expression of one family member increased sensitivity to ionic stress (Kim et al., 2001). There is evidence that one family member has a role in C and N metabolism and the plant hormone, abscisic acid (ABA), is involved in this response (Kang and Turano, 2003). Other family members may play a role in touch and cold sensing (Meyerhoff et al., 2005), growth of hypocotyls (Brenner et al., 2000) and roots (Sivaguru et al., 2003; Walch-Liu et al., 2006). For a role in sensing N status these receptors could detect amino acids in the phloem or apoplast and their cellular localization will be important in identifying this function.
Cytokinins and the His–Asp phosphorelay
There is evidence for the plant cytokinin hormones having a central role in signalling plant N status (Inoue et al., 2001), and these can be listed as follows.
- (i) The enzymes for the synthesis of cytokinins are specifically induced by NO supply and not other nutrients, although treatment with auxin can have a similar effect (Miyawaki et al., 2004).
- (ii) The concentrations of active cytokinins in plants changes in parallel with changes in N supply, for example, increasing when additional N is supplied (Takei et al., 2002); these changes can occur by synthesis or mobilization of stored forms.
- (ii) The concentrations of active cytokinins in plants changes in parallel with changes in N supply, for example, increasing when additional N is supplied (Takei et al., 2002); these changes can occur by synthesis or mobilization of stored forms.
Cytokinins signals are mediated by a multi-component phosphorylation system, composed of a histidine protein kinase (Kakimoto, 2003). Microarray analysis has identified a battery of over 200 genes that have many different functions that appear to be under the regulation of the cytokinin phosphorelay system (Kiba et al., 2005). The overlap between these genes and those responsive to changes in N status are candidates for a signalling role.
General amino acid control
This system is best understood in yeast, where amino acid biosynthetic pathways can be specifically induced by withholding supply of a specific N source (reviewed by Hinnebusch, 2005). In plants, several different components of a parallel system have been identified and, although the sequence homology is not always strong, some have been shown to complement the yeast mutants (Zhang et al., 2003). It therefore seems very likely that a similar control system for amino acid biosynthetic pathways exists in higher plants and gene knock-out mutants will be important tools for confirming this control system in plants. Yeast utilizes NH and amino acids directly as N sources so, assuming that the same general control system occurs in plants, it should be integrated with the regulation of NO uptake and assimilation and this must be a fundamental difference between the two types of organism. Therefore, fungi that can use NO like Hansenula sp. and Neurospora crassa, may be better model organisms for the situation in plants. In Neurospora, NIT2 a global transcription factor for responses to N has been identified and this protein has a zinc finger DNA-binding GATA domain that regulates the expression of the proteins needed to assimilate NO (Feng and Marzluf, 1998). Homologues have been found in plants (Daniel-Vedele and Caboche, 1993) and there is some complementation possible between the plant and fungal systems (Rastogi et al., 1997). The Arabidopsis GATA transcription factors are more implicated in light-mediated and circadian-regulated gene expression rather than the regulation of N metabolism (Manfield et al., 2007). A defect in the only nitrate-inducible GATA gene in Arabidopsis led to decreased chlorophyll content and down-regulation of the genes involved in sugar metabolism (Bi et al., 2005).
|
Cellular mechanisms for feedback regulation of N uptake |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
At the cellular level the simplest signal is likely to be a change in the compartmental pools of N, in particular the cytosol, as N influx occurs at the plasma membrane. Although changes in the phloem concentrations of amino acids may indicate a change in N status of the plant, it is actually within root cells where the signal must feedback to elicit changes in N uptake. Here we review what is known about changes in the cellular amino acid and NO
pools in relation to N supply.
Changes in cellular amino acid pools
There are few values reported for single cell amino acid concentrations and this is due to the technical difficulties associated with these types of measurements. When light and dark spinach leaf tissue was fractionated and compared, the cytosolic concentrations of most amino acids had increased considerably in the light (Winter et al., 1994). For example, Gln concentrations were reported to increase from 4.4 mM to 25.7 mM and yet when diurnal changes in NO influx by roots has been measured there is an increase in uptake during the light period (Macduff and Bakken, 2003). These changes in leaf amino acid cytosolic pools do seem compatible with the negative feedback model for NO uptake, unless the root is behaving differently. The resolution of this type of anomaly depends on obtaining improved methods for measuring cytosolic amino acid pools (e.g. FRET; Okumoto et al., 2005).
Changes in cellular nitrate pools
NO-selective microelectrodes were used to investigate the effect of treating barley roots with Gln (Fan et al., 2006). Cytosolic NO activities in root cortical and epidermal cells increased to a maximum after about 2 h, but by 6 h the activity was restored to a lower steady-state value (Fig. 2A). Treating roots with Gln for 6 h did not significantly change whole root tissue NO, but the pools of this amino acid did increase (Fig. 2B) and there was a decrease in the amount of active NO reductase (NR) in the root tissues (Fig. 2C). These parallel changes in root NR activity can provide an explanation for this change in cytosolic NO as this assimilatory sink for NO was decreased (Fan et al., 2006). The activity of NR is regulated by reversible Mg-dependent phosphorylation and binding of a 14-3-3 protein (Kaiser and Huber, 2001), which has been shown to be responsible for the observed light-regulated fluctuations in its activity in leaf tissue (Tucker et al., 2004). Furthermore, NO-selective microelectrode measurements on Arabidopsis leaf cells (Cookson et al., 2005) have also suggested that there is a strong dependence of cytosolic NO on NR activity. Although this idea does not seem compatible with results obtained using pieces of tobacco leaf which suggested that NO uptake at the plasma membrane can supply an increased rate of NO reduction (Lea et al., 2004). Furthermore, in a recent paper it was shown that there were significant differences in the leaf cytosolic NO pools of two rice cultivars that differed in their NUE (Fan et al., 2007). Changes in the cytosolic NO pool could provide a cellular signal indicating changes in N status and this is worthy of further investigation.
|
The changes in cytosolic NO
activity can act as a signal in plant cells; this does not necessarily imply a second messenger role, but can be a signal regulating gene expression and triggering the mobilization of other N pools (e.g. vacuolar NO; van der Leij et al., 1998). |
Future prospects |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
An exciting opportunity for unravelling the N signalling process in the future is provided by the use of specific gene mutants. For example, the Gln dumper mutants of Arabidopsis (Pilot et al., 2004), these plants exude excessive amounts of Gln that must be present in the apoplast and may therefore interfere with the usual N signalling systems. Studying the N physiology of these plants may provide useful information on the N signalling system. The fundamental link between N supply and growth is achieved through altering the transport and amounts of, as well as the sensitivity to, plant hormones as effectors for changing morphology. The role and importance of cytokinins in N status has been described (Inoue et al., 2001). Hormone mutants have been useful for the identification of the role in N signalling for responses such as ABA and lateral root growth (Signora et al., 2001). These tools are likely to continue to be very useful in the future, especially when used with plants that have altered N physiology and transport.
In agriculture and horticulture, N can be applied to the leaves of crops and the effects of these foliar inputs on signalling must be important. The consequences of these applications for N use efficiency by crops may be a significant target for genetic improvement as they do not reflect the usual site for N acquisition. By contrast, for some wild species of plants atmospheric deposition of N can negatively effect their distribution (Aber et al., 2003), but this result may be explained by competition for nutrients rather than a direct effect on signalling. Furthermore, the form of N application can be important in determining if the effect is positive or negative (Pearson and Stewart, 1993).
The N status of plants, and particularly the amino acid pools, must be closely linked to photosynthetic activity and the expression of some transporters depends on the amount of available carbon (Lejay et al., 2003). One interesting aspect of this feedback regulatory mechanism for N status is the change associated with plant development. For example, during senescence and remobilization of stored N pools the amino acids can increase and this will have knock-on effects for assimilatory enzymes such as NR and GS. This situation contrasts with that during early vegetative growth. These changes in plant development do not provide any problems for feedback regulation as the tissue and intracellular signals adjust appropriately. However, the regulatory targets for improving NUE during early vegetative growth will be very different from that at senescence.
|
Acknowledgements |
|---|
Rothamsted Research is grant-aided by the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK. Research in China was funded by the National Natural Science Foundation (grant numbers 30500309 and 30671234) and the National Basic Research Program 973 (grant No. 2005CB120903).
|
Abbreviations |
|---|
ABA, abscisic acid; FRET, Förster resonance energy transfer; Gln, glutamine; NUE, nitrogen use efficiency.
|
References |
|---|
|
TopAbstractIntroductionNitrate uptake by rootsAmmonium uptake by rootsAmino acid uptake by...Molecular nitrogen sensing...Cellular mechanisms for feedback...Future prospectsReferences |
|---|
Aber JD, Goodale CL, Ollinger SV, Smith ML, Magill AH, Martin ME, Hallett RA, Stoddard JL. Is nitrogen deposition altering the nitrogen status of northeastern forests? Bioscience (2003) 53:375–389.[CrossRef][Web of Science]
Andrews M, Raven J, Lea PJ, Sprent J. A role for shoot protein in shoot–root dry matter allocation in higher plants. Annals of Botany (2006) 97:3–10.
Arconedéguy T, Jack R, Merrick M. PII signal transduction proteins: pivotal players in microbial nitrogen control. Microbiology and Molecular Biology Reviews (2001) 65:80–105.
Beuve N, Rispail N, Laine P, Cliquet J-B, Ourry A, Le Deunff E. Putative role of gamma-aminobutyric acid (GABA) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant. Cell and Environment (2004) 27:1035–1046.[CrossRef]
Bi YM, Zhang Y, Signorelli T, Zhao R, Zhu T, Rothstein S. Genetic analysis of Arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. The Plant Journal (2005) 44:680–692.[CrossRef][Web of Science][Medline]
Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi GM. Arabidopsis mutants resistant to S(+)-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiology (2000) 124:1615–1624.
Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ. Futile transmembrane NH cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proceedings of the National Academy of Sciences. USA (2001) 98:4255–4258.[CrossRef]
Chiu J, Desalle R, Lam HM, Meisel L, Coruzzi G. Phylogenic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana. Molecular Biological Evolution (2002) 19:1066–1082.
Cookson SJ, Williams LE, Miller AJ. Light–dark changes in cytosolic nitrate pools depend on nitrate reductase activity in Arabidopsis leaf cells. Plant Physiology (2005) 138:1097–1105.
Cooper HD, Clarkson DT. Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals: a possible mechanism integrating shoot and root in the regulation of nutrient uptake. Journal of Experimental Botany (1989) 40:753–762.
Coutts G, Thomas G, Blakey D, Merrick M. Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO Journal (2002) 21:536–545.[CrossRef][Web of Science][Medline]
Crawford NM, Glass ADM. Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science (1998) 3:389–395.[CrossRef][Web of Science]
Daniel-Vedele F, Caboche M. A tobacco cDNA clone encoding a GATA-1 zinc-finger protein homologous to regulators of nitrogen metabolism in fungi. Molecular and General Genetics (1993) 240:365–373.
Dennison KL, Spalding EP. Glutamine-gated calcium fluxes in Arabidopsis. Plant Physiology (2000) 124:1511–1514.
Dluzniewska P, Gessler A, Kopriva S, Strand M, Novak O, Dietrich H, Rennenberg H. Exogenous supply of glutamine and active cytokinin to the roots reduces NO uptake rates in poplar. Plant. Cell and Environment (2006) 29:1284–1297.[CrossRef]
Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM. A role for glycine in the gating of plant NMDA-like receptors. The Plant Journal (2003) 35:800–810.[CrossRef][Web of Science][Medline]
Fan X, Gordon-Weeks R, Shen Q, Miller AJ. Glutamine transport and feedback regulation of nitrate reductase activity in barley roots leads to changes in cytosolic nitrate pools. Journal of Experimental Botany (2006) 57:1333–1340.
Fan X, Jia L, Li Y, Smith SJ, Miller AJ, Shen Q. Comparing nitrate storage and remobilization in two rice cultivars that differ in their nitrogen use efficiency. Journal of Experimental Botany (2007) 58:1729–1740.
Feng B, Marzluf GA. Interaction between major nitrogen regulatory protein NIT2 and pathway-specific regulatory factor NIT4 is required for their synergistic activation of gene expression in Neurospora crassa. Molecular Cell Biology (1998) 18:3983–3990.
Ferrario-Méry S, Besin E, Pichon O, Meyer C, Hodges M. The regulatory PII protein controls arginine biosynthesis in Arabidopsis. FEBS Letters (2006) 580:2015–2020.[CrossRef][Web of Science][Medline]
Ferrario-Méry S, Bouvet M, Leleu O, Savino G, Hodges M, Meyer C. Physiological characterization of Arabidopsis mutants affected in the expression of the putative regulatory protein PII. Planta (2005) 223:28–35.[CrossRef][Web of Science][Medline]
Forde BG. Local and long-range signaling pathways regulating plant responses to nitrate. Annual Review of Plant Biology (2002) 53:203–224.[CrossRef][Medline]
Fraisier V, Gojon A, Tillard P, Daniel-Vedele F. Constitutive expression of a putative high-affinity nitrate transporter in Nicotiana plumbaginifolia: evidence for post-transcriptional regulation by a reduced nitrogen source. The Plant Journal (2000) 23:489–496.[CrossRef][Web of Science][Medline]
Gansel X, Muños S, Tillard P, Gojon A. Differential regulation of the NO and NH transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant. The Plant Journal (2001) 26:143–155.[CrossRef][Web of Science][Medline]
Gessler A, Schultze M, Schrempp S, Rennenberg H. Interaction of phloem-translocated amino compounds with nitrate net uptake by the roots of beech (Fagus sylvatica) seedlings. Journal of Experimental Botany (1998) 49:1529–1537.
Henry HAL, Jefferies RL. Interactions in the uptake of amino acids, ammonium and nitrate ions in the Arctic salt-marsh grass, Puccinellia phryganodes. Plant. Cell and Environment (2003) 26:419–428.[CrossRef]
Hinnebusch AG. Translational regulation of GCN4 and the general amino acid pool control of yeast. Annual Review of Microbiology (2005) 59:407–450.[CrossRef][Web of Science][Medline]
Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W. Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. The Plant Cell (2006) 18:1931–1946.
Hodge A. Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytologist (2003) 157:303–314.[CrossRef][Web of Science]
Hsieh MH, Lam HM, van de Loo FJ, Coruzzi G. A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proceedings of the National Academy of Sciences. USA (1998) 95:13965–13970.[CrossRef]
Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature (2001) 409:1060–1063.[CrossRef][Medline]
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A. Dissolved organic nitrogen uptake by plants: an important N uptake pathway? Soil Biology and Biochemistry (2005) 37:413–423.[CrossRef]
Jones DL, Owen AG, Farrar JF. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biology and Biochemistry (2002) 34:1893–1902.[CrossRef]
Kaiser WM, Huber SC. Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. Journal of Experimental Botany (2001) 52:1981–1989.
Kakimoto T. Perception and signal transduction of cytokinins. Annual Review of Plant Biology (2003) 54:605–627.[CrossRef][Medline]
Kang JM, Turano FJ. The putative glutamine receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis. Proceedings of the National Academy of Sciences. USA (2003) 100:6872–6877.[CrossRef]
Kiba T, Naitou T, Koizumi N, Yamashino T, Sakakibara H, Mizuno T. Combinatorial microarray analysis revealing Arabidopsis genes implicated in cytokinin responses through the His
Asp phosphorelay circuitry. Plant and Cell Physiology (2005) 46:339–355.
Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG. Overexpression of the AtGluR2 gene encoding an arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant and Cell Physiology (2001) 42:74–84.
Kinraide TB, Newman IA, Etherton B. A quantitative simulation-model for H+-amino acid cotransport to interpret the effects of amino-acids on membrane-potential and extracellular pH. Plant Physiology (1984) 76:806–813.
Kobayashi M, Takatani N, Tanigawa M, Omata T. Post-translational regulation of nitrate assimilation in the cyanobactertium Synechocystis sp. PCC 6803. Journal of Bacteriology (2005) 187:498–506.
Krapp A, Fraisier V, Scheible WR, Quesada A, Gojon A, Stitt M, Caboche M, Daniel-Vedele F. Expression studies of Nrt2:1Np, a putative high-affinity nitrate transporter: evidence for its role in nitrate uptake. The Plant Journal (1998) 14:723–731.[CrossRef][Web of Science]
Kronzucker HJ, Glass ADM, Siddiqi MY. Inhibition of nitrate uptake by ammonium in barley. Analysis of component fluxes. Plant Physiology (1999) 120:283–291.
Lainé P, Ourry A, Boucaud J. Shoot control of nitrate uptake rates by roots of Brassica napus L. effects of localized nitrate supply. Planta (1995) 196:77–83.[Web of Science]
Lam HM, Chiu J, Hsieh MH, et al. Glutamate receptor genes in plants. Nature (1998) 396:125–126.[CrossRef][Medline]
Lea US, ten Hoopen F, Provan F, Kaiser WM, Meyer C, Lillo C. Mutation of the regulatory phosphorylation site in tobacco nitrate reductase results in high nitrite excretion and NO emission from leaf and root tissue. Planta (2004) 219:59–65.[CrossRef][Web of Science][Medline]
Lee R, Rudge K. Effects of nitrogen deficiency on the absorption of nitrate and ammonium by barley plants. Annals of Botany (1986) 57:471–486.
Lee RB, Purves JV, Ratcliffe RG, Saker LR. Nitrogen assimilation and the control of ammonium and nitrate absorption by maize roots. Journal of Experimental Botany (1992) 43:1385–1396.
Lejay L, Gansel X, Cerezo M, Tilliard P, Müller C, Krapp A, von Wirén N, Daniel-Vedele F, Gojon A. Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. The Plant Cell (2003) 15:2218–2232.
Loqué D, Lalonde S, Looger LL, von Wirén N, Frommer WB. A cytosolic trans-activation domain essential for ammonium uptake. Nature (2007) 446:195–198.[CrossRef][Medline]
Loqué D, von Wirén N. Regulatory levels for the transport of ammonium in plant roots. Journal of Experimental Botany (2004) 55:1293–1305.
Macduff J, Bakken A. Diurnal variation in uptake and xylem contents of inorganic and assimilated N under continuous and interrupted N supply to Phleum pratense and Festuca pratensis. Journal of Experimental Botany (2003) 54:431–444.
Manfield IW, Devlin PF, Jen C-H, Westhead DR, Gilmartin PM. Conservation, convergence, and divergence of light-responsive, circadian-regulated, and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family. Plant Physiology (2007) 143:941–958.
McIntyre GI. The role of nitrate in the osmotic and nutritional control of plant development. Australian Journal of Plant Physiology (1997) 24:103–118.[Web of Science]
Meyerhoff O, Müller K, Roelfsema M, Latz A, Lacombe B, Hedrich R, Dietrich P, Becker D. AtGLR3. 4, a glutamate receptor channel-like gene is sensitive to touch and cold. Planta (2005) 222:418–427.[CrossRef][Web of Science][Medline]
Miller AJ, Cookson SJ, Smith SJ, Wells DM. The use of microelectrodes to investigate compartmentation and the transport of metabolized inorganic ions in plants. Journal of Experimental Botany (2001) 52:541–549.
Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM. Nitrate transport and signalling. Journal of Experimental Botany (2007) 58:2297–2306.
Miyawaki K, Matsumoto-Kitano M, Kakimoto T. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. The Plant Journal (2004) 37:128–138.[CrossRef][Web of Science][Medline]
Moorhead GBG, Smith CS. Interpreting the plastid carbon, nitrogen, and energy status. A role for PII? Plant Physiology (2003) 133:492–498.
Muller B, Tilliard P, Touraine B. Nitrate fluxes in soybean seedling roots and their response to amino acids: an approach using 15N. Plant. Cell and Environment (1995) 18:1267–1279.[CrossRef]
Okumoto S, Looger LL, Micheva KD, Reimer RJ, Smith SJ, Frommer WB. Detection of glutamate release from neurons by genetically encoded surface-displayed FRET nanosensors. Proceedings of the National Academy of Sciences, USA (2005) 102:8740–8745.
Padgett P, Leonard R. Regulation of nitrate uptake by amino acids in maize cell suspension culture and intact roots. Plant and Soil 155/6, (1993) 159–161.
Pal'ove-Balang P, Mistrik I. Control of nitrate uptake by phloem-translocated glutamine in Zea mays L. seedlings. Plant Biology (2002) 4:440–445.[CrossRef]
Pearson J, Stewart GR. The deposition of atmospheric ammonia and its effects on plants. New Phytologist (1993) 125:283–305.[CrossRef][Web of Science]
Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U, Wingate VPM, Frommer WB. Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. The Plant Cell (2004) 16:1827–1840.
Quesada A, Krapp A, Trueman LJ, Daniel-Vedele F, Fernández E, Forde BG, Caboche M. PCR-identification of a Nicotiana plumbaginifolia cDNA homologous to the high-affinity nitrate transporters of the crnA family. Plant Molecular Biology (1997) 34:265–274.[CrossRef][Web of Science][Medline]
Rastogi R, Bate NJ, Sivasankar S, Rothstein SJ. Footprinting of the spinach nitrite reductase gene promoter reveals the preservation of nitrate regulatory elements between fungi and higher plants. Plant Molecular Biology (1997) 34:465–476.[CrossRef][Web of Science][Medline]
Raven J, Smith F. Nitrogen assimilation and transport in vascular land plants in relation to intracellular pH regulation. New Phytologist (1976) 76:415–431.[CrossRef][Web of Science]
Rawat SR, Silim SN, Kronzucker HJ, Siddiqi MY, Glass ADM. AtAMT1 gene expression and NH uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. The Plant Journal (1999) 19:143–152.[CrossRef][Web of Science][Medline]
Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiology (2004) 136:2483–2499.
Signora L, De Smet I, Foyer CH, Zhang HM. ABA plays a central role in mediating them regulatory effects of nitrate on root branching in Arabidopsis. The Plant Journal (2001) 28:655–662.[CrossRef][Web of Science][Medline]
Sivaguru M, Pike S, Gassmann W, Baskin TI. Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant and Cell Physiology (2003) 44:667–675.
Smith CS, Weljie AM, Moorhead GBG. Molecular properties of the putative nitrogen sensor PII from Arabidopsis thaliana. The Plant Journal (2003) 33:353–360.[CrossRef][Web of Science][Medline]
Sokolovski SG, Meharg AA, Maathuis FJM. Calluna vulgaris root cells show increased capacity for amino acid uptake when colonized with the mycorrhizal fungus Hymenoscyphus ericae. New Phytologist (2002) 155:525–530.[CrossRef][Web of Science]
Soldal T, Nissen P. Multiphasic uptake of amino acids by barley roots. Physiologia Plantarum (1978) 43:181–188.[CrossRef]
Stitt M. Nitrate regulation of metabolism and growth. Current Opinion in Plant Biology (1999) 2:178–186.[CrossRef][Web of Science][Medline]
Sugiyama K, Hayakawa T, Kudo T, Ito T, Yamaya T. Interaction of the N-acetylglutamine kinase with a PII-like protein in rice. Plant Cell Physiology (2004) 45:1768–1778.
Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H. Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. Journal of Experimental Botany (2002) 53:971–977.
Thornton B. Inhibition of nitrate influx by glutamine in Lolium perenne depends upon the contribution of the HATs to the total influx. Journal of Experimental Botany (2004) 55:761–769.
Tucker DE, Allen DJ, Ort DR. Control of nitrate reductase by circadian and diurnal rhythms in tomato. Planta (2004) 219:277–285.[CrossRef][Web of Science][Medline]
Trewavas AJ. Nitrate as a plant hormone. British Plant Growth Regulator Group Monograph (1983) 9:97–110.
Van der Leij M, Smith SJ, Miller AJ. Remobilization of vacuolar stored nitrate in barley root cells. Planta (1998) 205:64–72.[CrossRef][Web of Science]
Vidmar JJ, Zhuo D, Siddiqi MY, Schoerring JK, Touraine B, Glass ADM. Regulation of high affinity nitrate transporter genes and high affinity nitrate influx by nitrogen pools in plant roots. Plant Physiology (2000) 123:307–318.
Walch-Liu P, Liu L-H, Remans T, Tester M, Forde BG. Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant and Cell Physiology (2006) 47:1045–1057.
Watson R, Fowden L. The uptake of phenylalanine and tyrosine by seedling root tips. Phytochemistry (1975) 14:1181–1186.[CrossRef][Web of Science]
Westcott MP, Rosen CJ, Inskeep WP. Direct measurement of petiole sap nitrate in potato to determine crop nitrogen status. Journal of Plant Nutrition (1993) 16:515–521.[Web of Science]
Winter H, Robinson D, Heldt H. Subcellular volumes and metabolite concentrations in spinach leaves. Planta (1994) 193:530–535.[CrossRef][Web of Science]
Xu X, Ouyang H, Kuzyakov Y, Richter A, Wanek W. Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant and Soil (2006) 285:221–231.[CrossRef][Web of Science]
Yuan L, Loque D, Ye F, Frommer WB, von Wirén N. Nitrogen-dependent post-transcriptional regulation of the ammonium transporter AtAMT1;1. Nature (2007) 143:732–744.
Zhang Y, Dickson JR, Paul MJ, Halford NG. Molecular cloning of an Arabidopsis homologue of GCN2, a protein kinase involved in co-ordinated response to amino acid starvation. Planta (2003) 217:668–675.[CrossRef][Web of Science][Medline]
Zhou JJ, Theodoulou FL, Muldin I, Ingemarsson B, Miller AJ. Cloning and functional characterization of a Brassica napus transporter which is able to transport nitrate and histidine. Journal of Biological Chemistry (1998) 273:12017–12033.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||