Journal of Experimental Botany, Vol. 52, No. 90001, pp. 435-443,
March 2001
© 2001 Oxford University Press
Nitrogen nutrition and the role of root–shoot nitrogen signalling particularly in symbiotic systems
University of Dundee, Dundee DD1 4HN, Scotland, UK
Received 9 May 2000; Accepted 24 August 2000
 |
Abstract |
|---|
 Top Abstract IntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
To obtain and concentrate reduced N from the environment, plants have evolved a diverse array of adaptations to utilize soil, biotic and atmospheric N. In symbiotic N2-fixing systems the potential for oversupply exists and regulation of activity to match demand is crucial. N status in plants is likely to be most strongly sensed in the shoot and signals translocated to the roots may involve phloem transported amino compounds or very low concentrations of specific signal molecules. The mechanism for sensing N status in plant cells is not understood at the molecular level although it may be expected to be similar in all plants. Mechanisms for the regulation of symbiotic N2 fixation may be very different in the different symbiotic types. Rhizobia, Frankia and cyanobacteria are all symbiotic with different species of plants and the provision of O2, carbohydrate or other nutrients may control symbiotic activity to varying extents in the different symbioses.
Key words: N status, regulation, Gunnera, Nostoc, Lotus, actinorhizal.
|
Introduction |
|---|
|
TopAbstractIntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
Novel strategies to obtain nitrogen from the environment have evolved in the plant kingdom many times. These include an array of wonderful trapping mechanisms to catch organisms from terrestrial, air, water, and soil environments, symbiotic associations with nitrogen-fixing micro-organisms, mycorrhizal associations, and parasitic plants interactions. Most plants utilize
, 
, urea, and amino acids as N substrates and responses to these compounds vary among species. Some have evolved strategies that favour one specific substrate or a combination of substrates. Most crop species grow optimally with a mixture of ammonium and nitrate, the latter generally being the most abundant N form in freely drained aerobic soil environments (Crawford and Glass, 1998
). becomes an increasingly important substrate on ammonia- fertilized soils or on poorly drained, acidic soils where nitrification by micro-organisms is limited (Rice and Pancholy, 1972).
Whatever the mode of nitrogen acquisition be it by physiological adaptation/association or direct uptake from the rhizosphere, some form of regulation is generally required to match N uptake and assimilation to the N demands of plant growth and storage. Imbalances in uptake and assimilation for N compounds do occur with frequently accumulating in leaves and recent work has identified a role for water in nitrate homeostasis (Cardenas-Navarro et al., 1999). Progress so far in understanding regulatory control is limited, particularly in the field of symbiotic nitrogen-fixing systems. The following is a review of the mechanisms for nitrogen uptake and regulation in plants with particular reference to symbiotic systems.
|
Uptake of nitrogen compounds from the rhizosphere |
|---|
|
TopAbstractIntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
Nitrate uptake
Considering the relative importance of nitrate as an N source for agricultural crops, much research has focused on the uptake and assimilation of this substrate. It is recognized that
acts as an important signal molecule for growth. Arabidopsis mutants have been used to demonstrate that there is a specific mechanism for sensing and inducing root proliferation towards local supplies in the rhizosphere (Forde and Zhang, 1998). Rao and Rains showed, by using specific protein and RNA synthesis inhibitors, that stimulates its own specific transport system which takes up using proton symporters (Rao and Rains, 1976). Research over the last two decades has led to the cloning of genes encoding the representatives of two families of nitrate-induced nitrate transporters (NRTs). An Nrt2 family contributes to a highly inducible, high affinity nitrate uptake system. The Nrt1 group appears to account for more general, low level nitrate uptake characterized by constitutive, although to some extent inducible gene expression (Crawford and Glass, 1998). Recent kinetic analysis using Xenopus oocytes expressing cloned Chl1, a nitrate transport gene from Arabidopsis, have identified a biphasic pattern of transport activity with the single transporter having Michaelis-Menten Km values of 50 µM and 4 mM (Liu et al., 1999). It is envisaged that there is subsequent compensatory down-regulation of these systems involving internal nitrogen metabolites as potential signal molecules which are cycled in the phloem (Imsande and Touraine, 1994; Marschner et al., 1997). In effect, this mechanism enables nitrogen demand to be met in accordance with plant growth. Reports on the molecular basis for the regulation of expression of the nitrate transporters has recently identified nitrate reductase as a possible regulator of Nrt1 expression (Lejay et al., 1999), and assimilatory products such as glutamine in controlling Nrt2 expression (Zhuo et al., 1999; Vidmar et al., 2000).
Uptake of ammonia
Ammonium-specific transporters have now also been isolated in plant root hairs (von Wiren et al., 2000). LeAMT1;1 and LeAMT1;2 assessed from root hair isolation in tomato plants were found to be differentially regulated, high affinity transporters. LeAMT1;1 is induced by N deficiency (interestingly coinciding with low in planta glutamine concentrations) whereas LeAMT1;2 is positively regulated by increased supply. Three different AMT1 genes have been identified in Arabidopsis with differing affinities permitting regulation at the transcriptional level (Gazzarrini et al., 1999). Work with AMT1 expression has also demonstrated feedback regulation by root glutamine (Rawat et al., 1999). The collective system forms an efficient mechanism for root hair acquisition from the rhizosphere.
Uptake of other forms of N
Some species native to cold climates with nitrogen-limited ecosystems such as the arctic sedge (Eriophorum vaginatum) will preferentially take up organic N forms by directly scavenging amino acids from the soil (Chapin et al., 1993). The specific transporters (AAPs) remain to be fully characterized although functional complementation analysis using known AAP genes from models such as yeast have identified several plant genes with potential amino acid transport roles (Fischer et al., 1998; Schulze et al., 1999).
Marschner has reviewed the uptake of urea and concluded that it enters plants and is hydrolysed by urease within cells (Marschner, 1995). Urea transporters have been characterized in bacterial (Siewe et al., 1998) and mammalian systems (Ripoche and Rousselet, 1996), and the kinetics of a urea/sodium symport described for the plant Chara (Walker et al., 1993).
Conversion of different forms of N to ammonium
In non-symbiotic nitrogen metabolism the which has been imported into the symplast is reduced to 
by nitrate reductase, another enzyme in the nitrate assimilation pathway which is regulated by its substrate (Beevers and Hageman, 1983). Cytosolic can induce toxic symptoms if allowed to accumulate by inhibiting vacuolar ATPase proton pumping (Nelson and Taiz, 1989). Consequently, it is quickly reduced to by nitrite reductase and then further assimilated into organic compounds.
As with the uptake of nitrate, all other N compounds obtained from the rhizosphere are also chemically converted to ammonium as a consistent start point for plant amino acid biosynthesis. Protonation of NH3 to will occur at physiological pH in most plants. Urea and amino acids that are taken up are rapidly broken down by their respective catabolic enzymes to yield .
|
Specialized N nutrition: plants with physiological adaptations/associations for nutrient acquisition |
|---|
|
TopAbstractIntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
Nitrogen uptake by mycorrhizas and transfer to plants
Research on the role of mycorrhizas in plant nutrition has concentrated on their importance for P, K and water. Both arbuscular and ectomycorrhizas play a crucial role in plant P nutrition, and N transfer has been demonstrated for arbuscular mycorrhizas (Barea et al., 1992
) and ectomycorrhizas (Finlay, 1996). In ericoid mycorrhizas, uptake and transfer of N from both soil ammonium and amino acid sources has been demonstrated (Leake and Read, 1991). On heathland ecosystems where acid mor soils dominate, fungi form a significant proportion of the soil biomass and so fungal wall components such as chitin and hexosamines become very valid sources of N in the soil complex. Some ericoid mycorrhizal species can certainly degrade and utilize these substrates. It has been shown that the N is transferred from mycorrhiza to plant enhancing the growth of the host (Kerley and Read, 1995).
Other ectomycorrhizal and ericoid species produce acid proteinases and can access complex N sources via external protein hydrolysis (Hutchison, 1990a; Finlay et al., 1992). It has been postulated that the dominance of ectomycorrhizal species over arbuscular species in northern hemisphere coniferous ecosystems is related to their capability of utilizing complex forms of N when N becomes a strongly limiting nutrient (Hogberg, 1990).
Nitrogen uptake in carnivorous and parasitic plants
Carnivory occurs in 10 families of plants and provides N, P and other nutrients. In general, N is absorbed as amino acids and ammonium following the release of proteases, although there are some interesting exceptions: N absorption from insects trapped on Roridula gorgonias has been demonstrated eloquently using natural abundance 15N methods (Midgley and Stock, 1998). In this case it was shown that the plant does not produce exogenous enzymes like the morphologically similar sundews (Ellis and Midgley, 1996) and that autolysis and microbial breakdown of the trapped insects releases nutrients for subsequent absorption by the plant.
Several N transporters have been isolated in Nepenthes pitcher plants. These include NaAMT1; an ammonium specific transporter on the lower digestive glands of the pitchers, NaAAP1; an amino acid transporter expressed in the bundle sheath cells surrounding the vascular tissue, and NaNTR1; a peptide transporter detected in pitcher phloem cells thought to be involved in nitrogen export and phloem loading (Schulze et al., 1999). Indeed, it now appears that the glands of pitcher plants are specialized for bi-directional transport (Owen et al., 1999) although this hypothesis has not yet been applied or tested across the range of carnivorous families.
Similarly, parasitism has evolved many times and occurs in 16 families of angiosperms with varying extents of host dependence (Musselman and Press, 1995). Most parasites form a haustorial complex with a xylem to xylem or xylem to parenchyma connection and receive N nutrition via an apoplastic connection with host xylem. This can represent or amino acid sources that are subsequently assimilated by the parasite (Press, 1995).
N2-fixing symbiotic systems
Symbiotic N2 fixation has evolved in 11 families of dicotyledons and in the cycads, pteridophytes and bryophytes. Three types of symbiotic bacteria are recognized; rhizobia, Frankia and heterocystous cyanobacteria. In each symbiosis, C is transferred from the host plant and respiration of the bacteria within a specialist structure provides energy and reductant for bacterial nitrogenase activity. NH3 produced in this process, equilibrates to and is available for transfer to the host. In general, the ammonium is assimilated within the symbiotic plant cells, which act to maintain a very low level of free NH3/, thus ensuring continued N2 fixation.
In most symbiotic systems it is generally accepted that the symbiont gives up its fixed nitrogen to the host as ammonia/ammonium. However, recent data has illustrated that organic N compounds such as alanine can be excreted from N2-fixing soybean nodule bacteroids under certain conditions (Allaway et al., 2000; Waters et al., 1998). A candidate for a peribacteroid membrane ammonium transporter to account for the channel-like transporter system elucidated by patch clamp techniques and described in full by Tyerman et al. (Tyerman et al., 1995) was recently reported and characterized. Isolated from soybean nodules, the function of GmSAT1 was based on the ability of the protein to complement an transport defect in a yeast mutant (Kaiser et al., 1998). This could have accounted for bacteroid export certainly in the leguminous systems. However, on further analysis (Marini et al., 2000) the GmSAT1 protein was found merely to interfere with the Mep suite of transporters in yeast which seems to enable uptake. In summary, an ammonium transporter for the peribacteroid membrane has yet to be characterized.
Assimilation of ammonium
Irrespective of the original source of N obtained by plant cells, is a key compound in many of the systems. Ammonia assimilation is therefore a central process and it occurs in the same fashion in all systems characterized. The first stage involves the ATP/NADPH dependent GS/GOGAT cycle, which produces glutamine and then glutamate in the nodules. Aspartate, asparagine and alanine are subsequently metabolized by amino and amido transferase enzymes from glutamine and other more complex N compounds may be synthesized from these. The assimilated compounds are subsequently exported in the xylem.
|
Xylem and phloem N transport |
|---|
|
TopAbstractIntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
A wide variety of N compounds have been characterized as the major compounds in the xylem sap of both symbiotic and non-symbiotic plants. Amino acids such as asparagine and glutamine are frequently the major components, and other compounds such as citrulline, ureides and
are all transported (Table 1). The suite of compounds present in the xylem sap of a plant is characteristic of the species, season and the form of the N nutrition. The composition of N in the phloem is more uniform, and typically a diverse range of amino acids can be detected with asparagine, glutamine, glutamate and aspartate the major abundant components (Table 2).
|
|
Feedback control in symbiotic systems
In parallel with
uptake and regulation, symbiotic systems require overall regulation to ensure N2 fixation matches plant N demand. Indeed it may be viewed as an essential requirement of symbiotic systems that feedback regulation occurs, as symbiotic N2 fixation has the potential for oversupply leading to an inefficient system.
Sensing N status in plants
A single overriding mechanism for sensing N status in plants is not recognized. Undoubtedly the regulation and expression of many systems is regulated by components of N metabolism in plants, but understanding which chemicals are involved is crucial. The relative abundance of glutamine, glutamate and 2-oxoglutarate can be expressed as a ratio similar to Atkinson's (Atkinson, 1968, in Atkinson, 2000) treatment of adenylate charge, to provide a ‘nitrogen charge’ measure within a cell. This may represent a physiologically meaningful ratio that, via metabolite interactions with enzymes and gene expression directly affect N metabolism.
 |
Other key compounds that may be involved in N status recognition in cells include N rich compounds such as arginine and citrulline. Both these chemicals are not only components of primary N metabolism, but are also observed to accumulate under conditions of high N status.
Comparisons with yeast
Current understanding of N status and N signalling in plants is likely to be led by work on yeast as the physiology and genetics of these eukaryotes is studied as a model system. Murray et al. have concluded that the sensing and initial signalling of the availability or quality of N sources in yeast is not well understood (Murray et al., 1998). They have presented data showing that a glutamine tRNA (isoform tRNACUG) is involved in signalling N status for activities such as catabolite gene expression and sporulation. Further work with this signalling mutant (Beeser and Cooper, 1999) has supported its role in pseudohyphal growth, but questioned its affect on catabolite repression. The involvement of such a novel compound in N signalling pathways in a eukaryote is fascinating and may provide important insights into N status sensing and signalling in plants.
Autoregulation nitrate regulation and feedback regulation of nodulation and nitrogen fixation
In parallel with other disciplines, care is required to define the actual processes identified using particular keywords. Autoregulation is taken as describing the automatic control of further nodule development on a plant following inoculation with a compatible bacterium. This was elegantly demonstrated (Kosslak and Bohlool, 1984) using a split root experiment with delayed inoculation to the second split. This resulted in very few nodules developing on the delayed side, even after only 4 d. The response occurred before actual N2-fixing activity, by the nodules forming on the roots first inoculated, had begun. Mutant plants deficient in the autoregulation signalling pathway have been isolated (Carroll et al., 1985) and roots of these plant become covered in nodules (supernodulation) as suppression of nodule development does not occur. Interestingly, nodulation of these plants is insensitive to nitrate fertilization and for the Bragg soybean cultivar, grafting studies have shown it is the genotype of the shoot that regulates the appearance of supernodulation on the roots (Delves et al., 1986).
|
Case studies of different systems |
|---|
|
TopAbstractIntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
Three case studies are presented to demonstrate current understanding and introduce experimental systems to investigate the role of N status and signalling in different N2-fixing systems.
Case study 1. Lotus/Rhizobium
Over the last decade Lotus japonicus has become a useful model for determinate noduled legume physiology and molecular genetics studies whilst Medicago truncatula is also well established as a model species of equal value for indeterminate legume studies. Lotus is the diploid member of the Lotus corniculatus (birdsfoot trefoil) group of the genus with natural distributions recorded in eastern Asia (Taiwan, Korea, and Japan) extending as far west as Pakistan (Grant and Small, 1996). Under propagation it is easy to germinate, self-fertile, and will complete a seed setting life cycle in just 12 weeks when grown under optimal conditions, making it a rapidly growing and reliable research tool. Stougaard and Handberg at the University of Aarhus, Denmark pioneered and developed much of the now well-established Lotus transformation and culture methodology. Several Agrobacterium tumefaciens- mediated transformation procedures are now established in the literature which include hypocotyl infection and callus regeneration (Handberg and Stougaard, 1992; Handberg et al., 1994), hairy root infection (Stiller et al., 1997), and direct infection and regeneration from seedling cotyledon attachment sites (Ogar et al., 1996).
As a novel approach to understanding more about the relative importance of cycled amino compounds in feedback control of nitrogen fixation, a system is being developed for Lotus-based transformation systematically to alter the expression of some of the genes involved in amino acid transamination. This will enable the investigation of which compounds specifically act as signal molecules of N status which are sensed at the nodules and transduced to modulate changes in nodule turnover and N2-fixing activity in response to N demand. Initial trials on Lotus nodules show regulatory responses through both nitrogenase activity and nodule development under different N regimes (Fig. 1). Nodule growth in particular was shown to be highly inducible in Lotus under N-starved conditions. There are obvious parallels that can be made here to the regulation of nitrate uptake from the soil environment so the implications of this research may have much broader implications on plant nitrogen nutrition. An interesting observation in a report by Knight and Langston-Unkefer noted that alfalfa plants showed enhanced N2 fixation when infected by a plant pathogen which releases a glutamine synthetase (GS) inhibiting toxin (Knight and Langston-Unkefer, 1988). This may offer supporting evidence for a feedback response involving cycled organic N in that GS inhibition in the transamination pathway may render the subject incapable of sensing its own N status by depleting or upsetting the normal pool of cycled amino compounds.
|
Case study 2. Actinorhizal plants/Frankia
Actinorhizal plants are characterized by the diversity of plants that form symbiotic root nodules with Frankia. Although there are only some 220 species, they occur in 25 genera across eight plant families. The physiology of the nodule symbioses is similarly diverse with a range of nodule morphologies characterized, which in turn are related to the regulation of oxygen diffusion to the symbiotic Frankia (Abeysekera et al., 1990). Carbon translocation to actinorhizal nodules will occur in the phloem, and is frequently sucrose. Nitrogen translocation occurs as citrulline in Alnus (Wheeler and Bond, 1970) and Casuarina equisetifolia (Walsh et al., 1984), while in Casuarina cunninghamiana arginine is the single most abundant N compound (Sellstedt and Atkins, 1991). In most other actinorhizal plants examined, including Myrica, Hippophae, Ceanothus, and Elaeagnus, the amides glutamine and asparagine are common amino acids (reviewed by Huss-Danell, 1990).
The form of nitrogen translocated is recognized to be due to the genotype of the plant (Huss-Danell, 1990) and further control of plant N status will also be plant regulated. In a manner similar to legumes, actinorhizal plants have been shown to regulate nodule formation and activity to match N demand (Stewart and Bond 1961; Baker et al., 1997). However, as for legumes, understanding the exact mechanism of the plant sensing and signalling of N status remains to be discovered. It can be hypothesized that sensing may occur in cells present in the shoots (where N uptake mechanisms are integrated, free from sources of N), and that signals are returned to nodules and root systems via the phloem. From the observed responses of nodulated plants, it can be predicted that these signals operate in a quantitative manner, permitting N uptake and N2 fixation to be matched accurately to demand.
Nitrogen fixation in the nodules may be altered by the plant regulating the supply of carbon to the symbiotic Frankia. However, a limitation to current understanding of this process, is that the form of C transferred between plant and bacteria has not been determined in any actinorhizal system. The organic acids malate and succinate are recognized as forming the predominant form of C transferred in legume systems (Day and Copeland, 1991) and the sugars glucose, fructose and sucrose support Nostoc activity in Gunnera (see below). The need for further studies of the exchange of C in actinorhizal nodules was highlighted (Huss-Danell, 1990), and this challenge remains outstanding.
Case study 3. Gunnera/Nostoc
Gunnera species are the only angiosperms that form a symbiosis with cyanobacteria and they exist outside the traditional grouping of plants that form root nodules (Soltis et al., 1995). However, the Gunnera/Nostoc symbiosis is a complex system in which the Nostoc exist intracellularly within the stem tissue of Gunnera and this is characteristic of all 40 species of Gunnera. The bacteria appear to be non-specialized Nostoc punctiforme and once in symbiosis their metabolism is altered to become efficient symbionts. The heterocyst frequency increases to approximately 50% and the bacteria no longer fix CO2 or release O2 in the light. However, chlorophyll synthesis continues and light stimulates nitrogen fixation of isolated bacteria (Silvester et al., 1996).
Regulation in the Gunnera/Nostoc symbiosis:
Fixed N is released from the bacteria as (Silvester et al., 1996) and nitrogenase activity in isolated Nostoc is supported by exogenous sucrose, glucose or fructose (Fig. 2). An investigation of the levels of sugars present in symbiotic tissue when Gunnera was exposed to 100% oxygen for 4 h to destroy the symbiotic Nostoc nitrogenase activity showed in excess of twice the concentration of glucose, fructose and sucrose (assayed by GC-MS) than that in control treatments. In this system, where oxygen diffusion is largely restricted by the heterocyst envelope, regulation of the symbiosis must involve plant control of metabolites, or signals to the bacteria. It can be hypothesized that the availability of sugars is altered to match the N requirements of the plant. However, it is still not understood how the cyanobacterium is induced to produce a very high ratio of heterocysts, fix N2 in excess and release this N as ammonia for assimilation by the plant. Nostoc may represent a unique symbiont, in that it may not have additional ‘symbiotic’ genes and it may only exist in symbiosis because the plant hijacks its metabolism by placing it in conditions that induce the symbiotic state. The physical and chemical signals that bring this about remain to be determined. Support for this hypothesis may be obtained from molecular studies of diversity of symbiotic cyanobacteria (Rasmussen and Svenning, 1998) which show no clear separation of symbiotic and free-living isolates of Nostoc. Evidence to support the hypothesis that symbiotic Nostoc does not possess any specialist symbiotic genes will also be difficult to obtain. Isolates of specific tagged mutants that lack the ability to form symbiosis would permit the identification of putative symbiotic genes.
|
|
Summary |
|---|
|
TopAbstractIntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
The regulation of root activity to supply plants with adequate N is recognized to involve feedback systems, such that the N status of the whole plant influences root growth, transport activity and, in the case of plants with root nodules, nodule growth and activity. The precise signals that carry plant N status to nodules are unknown, but the route is almost certainly the phloem and likely candidates are N-rich amino acids that are translocated from the shoot. The control of root nodule activity in response to N status is likely to be achieved in different mechanisms in different plants. In the Gunnera/Nostoc symbiosis carbon transfer to the bacteria as sugars may be restricted when N is abundant, while in legume systems evidence exists that O2 gas diffusion is closely regulated and can restrict nodule activity when N is available. In actinorhizal plants, with Frankia as a symbiont, control may be via carbohydrate availability or O2 diffusion depending on the symbiosis. However, before characterizing the regulation of these symbioses it is necessary to understand how C is transferred and data have been presented to show the authors' recent progress in this work. Together, these examples illustrate efficient feedback systems that have evolved to regulate biological activity to match demand.
|
Acknowledgments |
|---|
We wish to thank BBSRC for studentship grant support and Lorraine Kay for providing the data relating to the Gunnera/Nostoc symbiosis. We also wish to acknowledge the useful comments of two expert referees.
|
Notes |
|---|
1 To whom correspondence should be addressed. Fax: +44 1382 322318. R.parsons{at}dundee.ac.uk
|
References |
|---|
|
TopAbstractIntroductionUptake of nitrogen compounds...Specialized N nutrition: plants...Xylem and phloem N...Case studies of different...SummaryReferences |
|---|
Abeysekera RM, Newcomb W, Silvester WB, Torrey JG. 1990. A freeze-fracture electron-microscopic study of Frankia in root nodules of Alnus incana grown at three oxygen tensions. Canadian Journal of Microbiology 36, 97–108.
Allaway D, Lodwig EM, Crompton LA, Wood M, Parsons R, Wheeler TR, Poole PS. 2000. Identification of alanine dehydrogenase and its role in mixed secretion of ammonium and alanine by pea becteroids. Molecular Microbiology 36, 508–515.[Web of Science][Medline]
Allen S, Smith JAC. 1986. Ammonium nutrition in Ricinis communis: its effect on plant growth and the chemical composition of the whole plant, xylem and phloem saps. Journal of Experimental Botany 37, 1599–1610.
Atkinson DE. 2000. The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7, 4030–4034.
Baker A, Dodd CD, Parsons R. 1996. Identification of amino compounds synthesized and translocateed in symbiotic Parasponia. Plant, Cell and Environment 19, 1249–1260.
Baker A, Hill GF, Parsons R. 1997. Alteration of N nutrition in Myrica gale induces changes in nodule growth, nodule activity and amino acid composition. Physiologia Plantarum 99, 632–639.
Barea JM, Azcon R, Azcon-Aguilar C. 1996. The use of 15N to assess the role of VA mycorrhiza in plant N nutrition and its application to evaluate the role of mycorrhiza in restoring Mediterranean ecosystems. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ, eds. Mycorrhizas in ecosystems. Cambridge: Academic Press, 190–197.
Beeser AE, Cooper TG. 1999. Control of nitrogen catabolite repression is not affected by the tRNAGln–CUU mutation, which results in constitutive pseudohyphal growth of Saccaromyces cerevisiae. Journal of Bacteriology 181, 2472–2476.
Beevers L, Hageman RH. 1983. Uptake and reduction of nitrate: bacteria and higher plants. In: Lauchli A, Bielski RL, eds. Inorganic plant nutrition (Encyclopedia of plant physiology, New Series, Vol. 15A). Berlin: Springer-Verlag, 351–375.
Cardenas-Navarro R, Adamowicz S, Robin P. 1999. Nitrate accumulation in plants: a role for water. Journal of Experimental Botany 50, 334, 613–624.
Carrol BJ, McNeil DL, Gresshoff PM. 1985. A supernodulation and nitrate tolerant symbiotic (nts) soybean mutant. Plant Physiology 78, 34–40.
Chapin FSI, Moilanen L, Kieland K. 1993. Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361, 150–153.
Crawford NM, Glass ADM. 1998. Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 3, 389–395.[Web of Science]
Day DA, Copeland L. 1991. Carbon metabolism and compartmentation in nitrogen-fixing legume nodules. Plant Physiology and Biochemistry 29, 185–201.[Web of Science]
Delves AC, Mathes A, Day DA, Carter AS, Carrol BJ, Gresshoff PM. 1986. Regulation of Rhizobium–soybean symbiosis by shoot and root factors. Plant Physiology 82, 588–590.
Ellis AG, Midgley JJ. 1996. A new plant–animal mutualism involving a plant with sticky leaves and a resident hemipteran insect. Oecologia 106, 478–481.
Finlay RD. 1996. Uptake and translocation of nutrients by ectomycorrhizal fungal mycelia. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ, eds. Mycorrhizas in ecosystems. Cambridge: Academic Press, 91–97.
Finlay RD, Frostegard A, Sonnerfeldt AM. 1992. Utilization of organic and inorganic nitrogen sources by ectomycorrhizal fungi in pure culture and in symbiosis with Pinus contorta Dougl. ex Loud. New Phytologist 120, 105–115.
Fischer WN, Andre B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB. 1998. Amino acid transport in plants. Trends in Plant Science 3, 188–194.[Web of Science]
Forde B, Zhang H. 1998. Response: nitrate and root branching. Trends in Plant Science 3, 204–205.
Gardner IC, Leaf G. 1960. Translocation of citrulline in Alnus glutinosa.Plant Physiology 35, 948–950.
Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wiren N. 1999. Three functional transporters for the constitutive, diurnally regulated and starvation-induced uptake of ammonium into Arabidopsis roots. The Plant Cell 11, 937–947.
Grant WF, Small E. 1996. The origin of the Lotus corniculatus (Fabaceae) complex: a synthesis of diverse evidence. Canadian Journal of Botany 74, 975–989.
Handberg K, Stiller J, Thykjaer T, Stougaard J. 1994. Transgenic plants: Agrobacterium- mediated transformation of the diploid legume Lotus japonicus. In: Cell biology: a laborotatory handbook. Academic Press Inc, 119–127.
Handberg K, Stougaard J. 1992. Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. The Plant Journal 2, 487–496.[Web of Science]
Hogberg P. 1990. 15N natural abundance as a possible marker of the ectomycorrhizal habit of trees in mixed African woodlands. New Phytologist 115, 483–486.
Huss-Danell K. 1990. The physiology of actinorhizal root nodules. In: Schwintzer CR, Tjepkema JD, eds. The biology of Frankia and actinorhizal plants. London: Academic Press, 129–156.
Hutchison L. 1990. Studies on the systematics of ectomycorrhizal fungi in axenic culture. II. The enzymatic degredation of selected carbon and nitrogen compounds. Canadian Journal of Botany 68, 1522–1530.
Imsande J, Touraine B. 1994. N demand and the regulation of nitrate uptake. Plant Physiology 105, 3–7.[Web of Science][Medline]
Kaiser BN, Finnegan PM, Tyerman SD, Whitehead LF, Bergersen FJ, Day DA, Udvardi MK. 1998. Characterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules. Science 281, 1202–1206.
Kerley SJ, Read DJ. 1995. The biology of mycorrhiza in the Ericaceae.18. Chitin degradation by hymenoscyphus-ericae and transfer of chitin-nitrogen to the host- plant. New Phytologist 131, 369–375.
Knight TJ, Langston-Unkefer PJ. 1988. Enhancement of symbiotic dinitrogen fixation by a toxin-releasing plant pathogen. Science 241, 951–954.
Kossak RM, Bohool BB. 1984. Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiology 75, 125–130.
Layzell DB, Pate JS, Atkins CA, Canvin DT. 1981. Partitioning of carbon and nitrogen and the nutrition of root and shoot apex in nodulated legume. Plant Physiology 67, 30–36.
Leake JR, Read DJ. 1991. Proteinase activity in mycorrhizal fungi. 3. Effects of protein, protein hydrolysate, glucose and ammonium on production of extracellular proteinase by hymenoscyphus-ericae (Read) Korf and Kernan. New Phytologist 117, 309–317.
Lejay L, Tillard P, Lepetit M, Olive FD, Filleur S, Daniel-Vedele F, Gojon A. 1999. Molecular and functional regulation of two uptake systems by N- and C-status of Arabidopsis plants. The Plant Journal 18, 509–519.[Web of Science][Medline]
Liu KH, Huang CY, Tsay YF. 1999. CHL1 Is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. The Plant Cell 11, 865–874.
Marini AM, Springeal JY, Frommer WB, Andre B. 2000. Cross-talk between ammonium transporters in yeast and interference by the soybean SAT1 protein. Molecular Microbiology 35, 378–385.[Web of Science][Medline]
Marschner H. 1995. Mineral nutrition of higher plants. San Diego, Academic Press Limited.
Marschner H, Kirby EA, Engels C. 1997. Importance of cycling and recycling of mineral nutrients within plants for growth and development. Botanica Acta 110, 265–273.
Midgley JJ, Stock WD. 1998. Natural abundance of 
15N confirms insectivorous habit of Roridula gorgonias, despite it having no proteolytic enzymes. Annals of Botany 82, 387–388.
Murray LE, Rowley N, Dawes IW, Johnston GC, Singer RA. 1998. A yeast glutamine tRNA signals nitrogen status for regulation of dimorphic growth and sporulation. Proceedings of the National Academy of Sciences, USA 95, 8619–8624.
Musselman X, Press MC. 1995. Introduction to parasitic plants. In: Press MC, Graves JD, eds. Parasitic plants. London: Chapman and Hall, 1–13.
Nelson N, Taiz L. 1989. The evolution of H+-ATPases. Trends in Biological Sciences 14, 113–116.
Ogar P, Petit A, Dessaux Y. 1996. A simple technique for direct transformation and regeneration of the diploid legume species Lotus japonicus. Plant Science 116, 159–168.
Owen TP, Lennon KA, Santo MJ, Anderson AN. 1999. Pathways for nutrient transport in the pitchers of the carnivorous plant Nepenthes alata. Annals of Botany 84, 459–466.
Parsons R, Baker A. 1996. Cycling of amino compounds in symbiotic lupin. Journal of Experimental Botany 47, 421–429.
Pate JS, Atkins CA, Hamel K, McNeil DL, Layzell DB. 1979. Transport of organic solutes in phloem and xylem of a nodulated legume. Plant Physiology 63, 1082–1088.
Press MC. 1995. Carbon and nitrogen relations. In: Press MC, Graves JD, eds. Parasitic plants. London: Chapman and Hall, 103–124.
Rao KP, Rains DW. 1976. Nitrate absorption by barley. 1. Kinetics and energetics. Plant Physiology 57, 55–58.
Rasmussen U, Svenning MM. 1988. Fingerprinting of cyanobacteria based on PCR with primers derived from short and long tandemly repeated repetitive sequences. Applied and Environmental Microbiology 64, 265–272.
Rawat SR, Silim SN, Kronzucker HJ, Siddiqi MY, Glass ADM. 1999. AtAMT1 gene expression and uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. The Plant Journal 19, 143–152.[Web of Science][Medline]
Rice EL, Pancholy SK. 1972. Inhibition of nitrification by climax ecosystems. American Journal of Botany 59, 1033–1040.[Web of Science]
Ripoche P, Rousselet G. 1996. The urea transporters. Nephrologie 17, 383–388.[Web of Science][Medline]
Schulze W, Frommer WB, Ward JM. 1999. Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes. The Plant Journal 17, 637–646.[Web of Science][Medline]
Sellstedt A, Atkins CA. 1991. Composition of amino compounds transported in xylem of Casuarina sp. Journal of Experimental Botany 42, 1493–1497.
Siewe RM, Weil B, Burkovski A, Eggeling L, Kramer R, Jahns T. 1998. Urea uptake and urease activity in Corynebacterium glutamicum. Archives of Microbiology 169, 411–416.[Web of Science][Medline]
Silvester WB, Parsons R, Watt PW. 1996. Direct measurement of ammonia release and assimilation in the Gunnera–Nostoc symbiosis. New Phytologist 132, 617–625.
Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullen BC, Dowd JM, Martin PG. 1995. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, USA 92, 2647–2651.
Stewart WDP, Bond G. 1961. The effect of ammonium nitrogen on fixation of elemental nitrogen in Alnus and Myrica. Plant and Soil 14, 347–359.
Stiller J, Martirani L, Tuppale S, Chian R, Chiurazzi M, Gresshoff PM. 1997. High frequency transformation and regeneration of transgenic plants in the model legume Lotus japonicus. Journal of Experimental Botany 48, 1357–1365.
Tyerman SD, Whitehead LF, Day DA. 1995. A channel-like transporter for on the symbiotic interface of N2-fixing plants. Nature 378, 629–632.
Valle EM, Boggio SB, Heldt HW. 1998. Free amino acid composition of phloem sap and growing fruit of Lycopersicon esculentum. Plant Cell Physiology 39, 458–461.
Vidmar JJ, Zhuo D, Siddiqi MY, Schoerring JK, Touraine B, Glass ADM. 2000. Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiology 123, 307–318.
von Wiren N, Lauter FR, Ninemann O, Gillissen B, Walch-Lui P, Engels C, Jost W, Frommer WB. 2000. Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. The Plant Journal 21, 167–175.[Web of Science][Medline]
Walker NA, Reid RJ, Smith FA. 1993. The uptake and metabolism of urea by Chara australis. 4. Symport with sodium—a slip model for the high and low affinity systems. Journal of Membrane Biology 136, 263–271.[Web of Science][Medline]
Walsh KB, Ng BH, Chandler GE. 1984. Effects of nitrogen nutrition on xylem sap composition of the Casuarinaceae. Plant and Soil 81, 291–293.
Waters JK, Hughes II BL, Purcell LC, Gerhardt KO, Mawhinney TP, Emerich DW. 1998. Alanine, not ammonia, is excreted from N2 fixing soybean nodule bacteroids. Proceedings of the National Academy of Sciences, USA 95, 12038–12042.
Weber P, Stoermer H, Geßer A, Schneider S, von Sengbusch D, Hanemann U, Rennenberg H. 1998. Metabolic responses of Norway spruce (Picea abies) trees to long-term forest management practices and acute (NH4)2SO4 fertilization: transport of soluble non-protein nitrogen compounds in xylem and phloem. New Phytologist 140, 461–475.
Wheeler CT, Bond G. 1970. The amino acids of non-legume root nodules. Phytochemistry 9, 705–708.
Zhuo D, Okamoto M, Vidmar J, Glass ADM. 1999. Regulation of a putative high-affinity nitrate transporter (Nrt2,1At) in roots of Arabidopsis thaliana. The Plant Journal 17, 563–568.[Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  R. F. Grant, T. J. Arkebauer, A. Dobermann, K. G. Hubbard, T. T. Schimelfenig, A. E. Suyker, S. B. Verma, and D. T. Walters Net Biome Productivity of Irrigated and Rainfed Maize Soybean Rotations: Modeling vs. Measurements Agron. J., October 15, 2007; 99(6): 1404 - 1423. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Marino, P. Frendo, R. Ladrera, A. Zabalza, A. Puppo, C. Arrese-Igor, and E. M. Gonzalez Nitrogen Fixation Control under Drought Stress. Localized or Systemic? Plant Physiology, April 1, 2007; 143(4): 1968 - 1974. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||