1 APS402 Dissertation Candidate no: 000125738

Transport of nitrogen in plants

Kelly Simpson
Nitrogen plays a critical role in plant growth, as it is Nutrients enter the plant and move up the xylem by mass
required for the synthesis of amino acids, proteins and flow, this does not necessarily allow the nutrients to get to
DNA. Plants take up nitrate from the soil and by where they are needed. They must be transported from the
reduction convert it to ammonia. Plants can take up older leaves to shoots, fruits and other storage parts via the
ammonia directly from the soil but it is present in
much smaller quantities compared to nitrate.
phloem.
Ammonia can also be obtained by root nodules fixing
atmospheric nitrogen, by photorespiring leaves and
the phenylpropanoid pathway. Ammonia enters the

Photosynthesis
GS/GOGAT cycle where glutamate is assimilated from

Rate of
glutamine and oxoglutarate. The amino group is
transferred to other amino acids especially asparagine
which is one of the major nitrogen transporting
compounds in plants. Once asparagine is where it is
needed in the plant it is broken down so that proteins,
RNA and DNA can be synthesised. The main focus will Available Nitrogen in the Soil
be on asparagine and what occurs when it reaches the
sink tissue in plants. References will also be made to
the manipulation of asparagine metabolism in
arabidopsis and the possible role that PEPCK plays in Fig. 1. Nitrogen is one of the major limiting factors in
nitrogen metabolism. photosynthesis.

Ammonium at high concentrations is a toxic compound as

Nitrogenous compounds, their uptake and
it lowers the cells pH. Free ammonia can readily diffuse
transport in the plant
out of the plant, which would mean a loss of a valuable
On a dry matter basis the principal elements in higher resource. If ammonia is assimilated from nitrate it can not
plants are carbon, hydrogen, oxygen, nitrogen, potassium, be allowed to accumulate and can not be transported in its
sulphur and phosphorus [1]. Autotrophic higher plants original state it must be assimilated into amino acids or
obtain their carbon from the atmosphere, whilst the roots ureides (if a tropical legume). Not just any amino acid is
take up most of the nutrients with shoots absorbing some formed to transport nitrogen around the plant, a compound
mineral nutrients [2,3]. Nitrogen is the most important with a high N/C ratio, high solubility and low reactivity is
mineral nutrient for plants. The atmosphere contains 78% needed [4]. Glutamine, asparagine (Fig. 2.) and arginine
nitrogen but this source is only available to a few plants are examples of transport amides. Pate [5] found large
that have symbiotic relations with nitrogen fixing bacteria. concentrations of asparagine in the phloem and xylem, he
Instead plants depend upon soil minerals for their source determined that this was the plants main method of
of nitrogen. Scientists have discovered that photosynthesis transporting nitrogen from the source tissue to where it
is closely related to the nitrogen content in leaves. A high was needed e.g. from germinating seedlings and senescing
nitrogen supply causes a high rate of photosynthesis and leaves to fruit and growing leaves. In humans amino acids
so a faster rate of growth (Fig 1. As nitrogen increases form the main source of energy for the liver [6].
photosynthesis increases). Nitrogen is available to plants
either in the form of nitrate (NO3-), or ammonium (NH4+).
Unfortunately for plants nitrates are very soluble
compounds and are easily leached from the soil. For this
reason a deficiency in nitrogen is often a limiting factor to
plant growth. Leaching is not the only way nitrogen is
removed from the soils, nitrogen is essential for all life and
so plants and microorganisms compete for its acquisition.
Ammonia, ammonium and nitrate Fig. 2. The amide asparagine
Nitrate and ammonium can move from root to shoot
through the xylem along the transpirational stream. Ureides
Nitrogen can also be transported in the phloem but it is Ureides are nitrogen-containing compounds. The structure
normally in the form of amino acids and amides. of the ureide allantoin can be seen in Figure 3.
2 APS402 Dissertation Candidate no: 000125738

amides is glutamine and asparagine. The tropical legumes

Fig. 3. Allantoin is a ureides that contains four nitrogen
molecules and four carbon molecules
Examples of this compound are citrulline, allantoin and
allantoic acid. Tropical legumes use ureides as a transport
molecule because it takes less carbon to transfer the same
amount of nitrogen than the amide transporters. Soybean
and cowpeas are tropical legumes and transport organic
nitrogen as ureides when nodulated. Ureides are not a
universal method of transporting nitrogen due to the severe
draw back of being less efficient than using amides. In fact,
transport ureides in the xylem sap while temperate
legumes use amides, mainly asparagine, especially when
they are nodulated. It is possible in Lupin to decrease the
amount of asparagine in the xylem sap by exposing the
nodules to oxygen, this inhibits nitrogen fixation [7].
Schobert and Komor [8] suggested that the uptake of
amino acids in to the xylem was based on a selective
process, they compared the amino acid content of the
xylem with that of the root tissue in Ricinus and found that
there was a significant difference in the amino acid
composition. Pate [9] looked at uptake of nitrogenous
compounds in plants and found that the composition of the
xylem sap varied greatly among his group of monocot and
dicot plants (Fig. 4).
Xanthium

it is almost twice as expensive metabolically to use ureides Stellaria

instead of amides as catabolising ureides releases carbon Trifolium

as carbon dioxide. Another reason why ureides are not an Perilla

Avena
efficient transport method is that they are formed from Zea
Nitrate
purines which are themselves created from glutamine, Impatiens Amino Acids
glycine, aspartate and ribose-5-phosphate. The formation Helianthus
Amides
and subsequent breakdown of ureides is a very complex Hordeum
ureides
process requiring many cells and organelles to Phaseolus

communicate and work together. The production of urea Vicia

in animal systems also occurs through the activities of

Pisum

Raphanus
arginase and it has been suggested that the production of Lupinus

urea in this way provides a mechanism for the removal of

ammonia in a cyclic series of reactions originally proposed 0% 50% 100%
by Krebs and Henseleit in 1932.

Transport in the xylem Fig. 4. Relative proportions of nitrogen components of

Xylem sap can include inorganic nitrogen, ureides and xylem sap from a large representation of monocot and
amino acids. All amino acids are present in the xylem sap dicot plants. (Redrawn from Pate 1973[9])
but in varying concentrations, the major constituent of sap

Fig. 5. Movement of nitrogen in plants. The blue arrows show the movement of nitrogen in the phloem and xylem.
AA, Amino acids.

S y n th e s is a n d tr a n s fo r m a tio n
A A ’s
A m id e s O th e r A A ’s
U r e id e s >
N O 3
S e e d c o a t m e ta b o lis m

T r a n s fo r m a tio n S to r a g e
L eaf
o f A A ’s > p r o te in s

F r u it NO 3
-

A m id e s
> >
S y n th e s is A m id e s NH 4
+ NO 3
-
A A ’s
A A ’s
N 2 > NH 4
+
> U r e id e s

R o o ts
R o o t n o d u le
L egum e N o n le g u m e
3 APS402 Dissertation
Transport in the phloem
The phloem sap conveys the amino acids from mature
exporting leaves or from senescing leaves to the young
growing leaves and fruits, Delrot et al. [10]. In the same
way to the xylem the phloem can carry all of the amino
acids at varying concentrations, usually amino acids
account for 5-10% of the phloem sap solutes.
During circulation in the plant, selective transport
seems to occur between the xylem and phloem so that
solute concentration in the two remains quite different.
The xylem sap is not restricted to carrying just mineral
solutes but can transport sugars and organic solutes as well
even though the phloem is more adapted to do so.
Nitrogen metabolism is a key aspect of plant mineral
nutrition [11] and is essential for life processes. Amino
acids help form the building blocks for life and are vital
for proteins, enzymes and DNA.
Leaf senescence and the relocation of nitrogen
Senescence is described as the deteriative events which
proceed the death of a mature cell. Plants lose their leaves
either annually (synchronous senescence) of if coniferous
about every seven years (sequential senescence). The
internal constituents of the leaves must be broken down
and translocated to other parts of the plant so as to hold on
to precious resources. Photosynthetic proteins are a
valuable source of nitrogen so their breakdown and
removal from the leaf aids in the plants success [12]. It is
thought that senescence is brought about by a failure or
decreased ability for protein synthesis [13]. In ageing
senescing leaves aerobic catabolism of purines is thought
to be a method of nitrogen conservation by the plant. The
breakdown product-allantoic acid- is transported out of the
leaf and can be stored or utilised elsewhere in the plant.
The amino acids in seeds can be derived from a variety
of sources (Fig. 6). In annual plants the onset of fruit and
seed development is frequently accompanied by the
senescence of leaves in the plant. During the senescence
of leaves, proteins may be hydrolysed and the products
translocated to the developing seed and fruit.
Lipids
Protein
Carbohydrates
Via phloem
AA’s
Mg2+ Energy
Chlorophyl
Seeds, fruit or
Storage etc.
Fig. 6. Movement of compounds from a senescing
leaf to seeds, fruit and storage organs.
Candidate no: 000125738
Reduction of nitrate and nitrite to ammonia
Nitrate reductase Nitrite reductase
Nitrate Nitrite Ammonia
Nitrate reduction occurs in the cytoplasm of leaves and
roots. The reaction is induced by the presence of the
substrate and is inhibited by the production of ammonia.
The activity of the enzyme is regulated by light and
phosphorylation. Phosphorylation influences enzyme
activity [14], by allowing an inhibitor protein to bind to
the site of action. The small protein belongs to the 14-3-3
class of inhibitor proteins and is found in all major classes
of eukaryotes.
Nitrate reductase
NO3- + NAD(P)H + H+ NO2- + NAD(P)+ + H2O
Nitrite reduction occurs in the plastids of leaves and roots.
Nitrite and nitrate induce the activity of the enzyme. The
reductant is either a photosynthetically-generated
ferredoxin if in the chloroplast, or a ferredoxin-like
molecule if in the root plastids.
Nitrite reductase
NO2 + 6 ferredoxinred + 8 H+
-
NH4+ + 6
ferredoxinox + 2 H2O
All the compounds made in the above reactions are toxic
to varying degrees so assimilation must occur quickly to
prevent damage to the plant. It is thought that the balance
between leaf and root nitrate reduction may be closely
related to malate traffic in the phloem with potassium ions
balancing electrical charge on the way down (phloem) and
recirculating in the xylem.
The GS/GOGAT cycle converts ammonia by the
combined activity of glutamine synthetase and glutamate
synthase. In this cycle (Fig. 7) an amino group is added to
glutamate using ATP and the enzyme glutamine
synthetase. The extra amino group on the glutamine is
transferred using NADH or Fdred and is catalysed by
glutamine synthetase (glutamine-oxogluterate
aminotransferase GO/GAT) to oxoglutarate (a
dicarboxylic acid) to produce two molecules of glutamate.
One is recycled and the other can be stored or converted
into amino acids. Much of the nitrogen transported in the
xylem and the phloem is in the form of asparagine that has
been formed from glutamine. It is not possible to
generalise where the above reaction occurs because it
varies in from plant to plant.
4 APS402 Dissertation
NH4+
ATP ADP
Glutamine
synthetase
(GS)
Glutamate Glutamine
Glutamate
Synthase
(GOGAT)
Fdox Fdred
Or Or
NAD+ NADH + H+
Glutamate 2-Oxoglutarate
Fig. 7. The GS/GOGAT cycle. Ammonium from glutamate,
or aspartate can be incorporated in to the cycle not just
ammonium from the soil of from the reduction of nitrate. Fig. 8. A flow diagram showing the formation of
asparagine in plants using the enzymes a), Asparagine-
Asparagine
oxoacid transaminase, b), β-cyanonalanine synthase and
Vauquelin and Robiquet first discovered asparagine in c), asparagine synthetase [4].
1806 in Asparagus sativus. Asparagine is found to make
up a considerable portion of the amino acids that are
transported in the phloem, this is true for many species
including corn, pea, asparagus [4] and Arabidopsis [15].
Asparagine is a key compound synthesised for nitrogen
storage and transport particularly when carbon supplies are
limited [16]. It was noted [17,18] that the concentration of
asparagine in plants varied with light and dark, the
significance of this was unclear until in 1922
Prianischnikow observed that asparagine concentrations
increased in light in the presence of ammonia and
suggested that the accumulation of asparagine may be a
mechanism for ammonia detoxification. Asparagine is a
compound that has a low C:N ratio (2:1), high solubility
(more so than the ureides [19]) has great stability and
mobility in physiological fluids. Asparagine is the main
nitrogen constituent of the xylem sap in many varieties of
plants, with glutamine coming a close second.
There have been three methods proposed for the
synthesis of asparagine, the first occurs in animals and has
been identified in rat liver extracts and is thought to have a
similar reaction in plants, it involves the synthesis of
asparagine from 2-oxosuccinamic acid (OSA) and either
α-aminobutyric acid, alanine or glutamine [30] using the
reverse reaction of asparagine:oxoacid transaminase (Fig.
8a). The second reaction involves β-cyanonalanine
synthase (Fig. 8b) which catalyses the formation of β-
cyanonalanine from cyanide and cysteine. The product is
then hydrolysed using β-cyanonalanine hydolase
producing asparagine. The enzyme in this method has
been detected in many plant species [19] such as lupin,
sorghum and pea. However, this reaction occurs much
more readily in the opposite direction and so has been
suggested as a method of asparagine catabolism [4]. The
final pathway involves asparagine being synthesised by
asparagine synthetase (Fig. 8c) which catalyses the
amidation of aspartate by glutamine in an ATP-dependent
Candidate no: 000125738
reaction [20]. Many plants are found to contain asparagine
synthetase and the enzyme has been isolated in the
cotyledons of germinating seedlings, maize roots and root
nodules.
This enzyme controls the re-allocation of nitrogen during
specific developmental stages and environmental changes,
e.g. during seed development nitrogen is transported to the
seeds and in times of stress nitrogen is stored so that it is
not lost, this indicates that asparagine has a close
relationship with plant growth and development.
L-Glutamine + L-aspartate + ATP → L-asparagine + L-
glutamate + AMP + PPi
Manipulation of asparagine regulation in arabidopsis
There are three genes that code for the three isoenzymes of
asparagine synthetase in Arabidopsis thaliana, ASN1,
ASN2 and ASN3. In A. thaliana ASN1 is expressed
predominantly in the shoots. In several species, it has
been shown that mRNA accumulation of ASN1 is
repressed by light and/or sugar. This is consistent with the
observation that levels of free ASN change in light-versus
dark treated plants [14,16]. Lam also observed that ASN2
is expressed at low levels in the dark and its mRNA
accumulate preferentially in light treated plants. From this
information it would be expected that ASN1 and 2 would
be expressed in the leaves probably in the chloroplasts or
the plastids.
Previous studies have shown that overexpression of
ASN1 in Arabidopsis enhances the nitrogen status of seeds,
the ultimate storage organs for metabolites [21]. Overall
very little experimentation has been carried out in this area
of nitrogen assimilation control. Further research could be
carried out looking at the mechanisms of asparagine in the
In nitrate rich soils nitrogen metabolism usually occurs
in the leaves. The leaves provide a good site as they have
the necessary energy production due to photosynthesis and
also because they are a source of carbon skeletons. A
disadvantage to it occurring here is the production of
hydroxide ions, which will alter the pH of the leaf, to cope
5 APS402 Dissertation
with this the plant, produces organic acids so as to balance
the pH.
What happens when aspargine arrives at a sink
tissue?
Asparagine is a transport molecule to get nitrogen to
where it is needed in the plant. There are two confirmed
pathways suggested for the breakdown of asparagine, one
involving transamination (Fig. 9.), and the other
deamidation by asparaginase.
Deamidation L-Asparagine + H2O → L-Aspartate +
NH3
Transamination Asparagine + Oxo acid → Amino acid +
2-oxosuccinamate
Fig. 9. A flow diagram showing the movement of nitrogen
through the GS/GOGAT cycle and transamination to
produce amino acids and subsequently proteins [28]
Wilson et al. discovered asparagine transaminase in the
1950’s [22]. Transamination results in the redistribution
of nitrogen from asparagine to other amino acids.
Asparagine is needed for protein synthesis and it has been
suggested that it is involved in photorespiration [23]
Murray and Cordova-Edwards [24] studied asparagine
metabolism in peas and observed that the asparagine that
arrived at the fruits of the legumes was unmetabolised. In
the hull of the developing pea fruits the metabolism of
asparagine is relatively slow compared to that of glutamine.
It has been suggested [24,25] that the location for
asparagine metabolism is the seedcoat. Deamidation
involves the hydrolysis of asparagine by asparaginase to
produce aspartate and ammonia.
Where does the carbon go when asparagine is
catabolised – Krebs cycle or gluconeogenesis?
All of the amino acids except for two (leucine and lysine)
can be broken down in to Kreb cycle intermediates. This
allows the carbon skeleton of asparagine to be converted
to oxaloacetate and then to pyruvate. The fate of the
pyruvate depends on the cell energy charge. In cells with
a high-energy charge pyruvate is directed to
Candidate no: 000125738
gluconeogenesis. This occurs due to coenzyme A being
highly acylated mainly as acetyl-CoA, which activates
pyruvate carboxylase, directing pyruvate toward
gluconeogenesis. When the energy charge is low CoA is
not acylated and so pyruvate carboxylase is inactive,
pyruvate is oxidised to carbon dioxide and water by
pyruvate dehdrogenase and enzymes in the Kreb cycle.
Gluconeogenesis is the synthesis of glucose from other
metabolites and is essentially the reversal of the glycolysis
reaction. The process of gluconeogenesis is very costly in
terms of energy since two moles of pyruvate are needed to
form two moles of 1,3-bisphosphoglycerate consuming six
moles of ATP. In glycolysis only two moles of ATP are
formed from two moles of pyruvate synthesised from two
moles of glucose.
The Krebs cycle is of great importance in cell
biochemistry for three main reasons. 1, macromolecules
are degraded to carbon dioxide. 2, It produces hydrogen
atoms that provide the reducing power for the electron
transport chain and so is the source of metabolic energy
for the cell. 3, It provides the cell with valuable
intermediates that have the potential to be anabolised in to
other compounds (Fig. 10.).
Fig. 10. The Krebs cycle and it’s major anaplerotic and
caterplerotic functions [26]
Very little asparagine is secreted in to the embryo sac from
the seed coat, so it is surprising to find the label derived
from the asparagine carbon skeleton reassimilated in to
other compounds such as glutamine, alanine, sucrose and
valine in the embryo sac [24]. When Murray and
Cordova-Edwards [24] fed peas 14C labelled asparagine,
they found that glutamine was the major labelled form of
nitrogen transported from the seed coats to the embryo sac.
This gave clear evidence that asparagine and aspartate was
converted to glutamate and glutamine in the seed coats
(Fig. 11). Oxaloacetate (OAA) is formed by the removal
of an amide from asparagine using asparaginase and
6 APS402 Dissertation
aspartate: oxogluterate aminotransferase. In the
mitochondria OAA enters the Kreb cycle and by the action
of a number of enzymes forms oxoglutarate (OG). It is at
this stage that oxoglutarate could be converted via a
reaction catalysed by aminotransferase to glutamate which
in turn can be transformed in to glutamine via glutamine
synthetase. It was also shown in this experiment that the
conversion of asparagine to glutamine declined in the seed
coats after the volume of embryo sac liquid had declined
and that there was an increase in the amount of asparagine
that provided the embryo with nitrogen. At this time there
was still a conversion of asparagine to glutamate and
glutamine in the seed coats and the embryo but with
favouritism shown for glutamate.
Fig. 11. Conversion of asparagine (ASN) to glutamate
(GLU) and glutamine (GLN) using the following enzymes: 1
asparaginase, 2 aspartate: oxogluterate aminotransferase,
3 condensing enzyme, 4 aconitase, 5 isocitrite
dehydrogenase, 6 glutamine synthetase. [24].
Where does the nitrogen go when Asparagine is
catabolised?
Once the asparagine has got to its sink tissue it can be
stored, converted to other amino acids by tranamination as
mentioned earlier or broken down to aspartate or even
further down to ammonia.
Storage can be either short or long term. Nitrate,
amino acids and vegetative storage proteins are
compounds used to store nitrogen over the short term.
They are located in stems or leaves and this type of storage
occurs when there is a plentiful supply of exogenous
nitrogen and it exceeds the plants nitrogen demand.
Asparagine and glutamine can be stored in the vacuoles of
leaf cells, other amino acids can be stored but it is mainly
the two mentioned above.
Long-term storage is used by the plant as a means of
conserving nitrogen and even occurs at times of nitrogen
deprivation. The plants need to store nitrogen competes
with the demand of growing organs for nitrogen. Tromp
[27] observed that amino acids are involved in long-term
storage but that they were mainly incorporated in to
proteins. Proteins constitute the main form of long term
storage in leaves, bark of trees, cereal and legume seeds.
A major sink of nitrogen is chlorophyll and photosynthetic
proteins. It has been suggested that Rubisco can hold 25%
Candidate no: 000125738
of nitrogen in C3 plants and can account for 50% of the
soluble protein content of C3 leaves.
Seeds accumulate nitrogen as seed storage proteins, the
type of protein is dependent on the species of plant. Seed
storage proteins lack any other biological activity except to
provide the seed with a supply of nitrogen sulphur and
carbon skeletons for the developing seedling [28].
In humans the liver can not utilise all the ATP that
would be produced if all the amino acids were oxidised to
CO2. The carbon skeletons from these amino acids are
converted to glucose by gluconeogenesis. The ATP that is
needed for this to occur comes from the surplus of ATP
produced when amino acids are oxidised [6]
Possible role for PEPCK in nitrogen metabolism
PEPCK (phosphoenolpyruvate carboxykinase) is known to
play a part in gluconeogenesis, in developing seeds and in
leaves of C4 and CAM plants. It has been suggested [26]
that PEPCK is involved in the cataplerosis of
intermediates in the Kreb cycle that are there in excess due
to the catabolism of amino acids. PEPCK catalyses the
reaction that forms phosphoenolpyruvate (PEP) from OAA
(fig. 10.). Once PEP is formed it can either be used to
create sugars by gluconeogenesis or converted to pyruvate
which can then re-enter the Kreb cycle.
PEPCK
OAA PEP
Walker et al. [34] observed that when grape seeds were
fed asparagine there was an increase in the presence of
PEPCK. The production of PEPCK was asparagine
specific as when aspartate or ammonia was fed to the plant
there was no such induction. The catabolism of amides
and the integration of these products in to the Kreb cycle
has an anaplerotic effect, as intermediates are taken out for
biosynthesis they must be replaced. Just as the
intermediates need to be replaced so does acetyl CoA, this
can occur by either PEPCK or NAD(P)-malic enzyme
depending on the type of plant, and then the subsequent
transformation of PEP to pyruvate and then to acetyl CoA.
Conclusion
Nitrogen plays a critical role in plant growth, as it is
required for the synthesis of amino acids, proteins and
DNA. The movement of nitrogen around the plant is a
highly controlled process, and the assimilation and
metabolism of nitrogenous compounds requires the
presence of many enzymes. The amide asparagine has
been shown to be essential in the transport and storage of
nitrogen in higher plants. Genetic studies of asparagine in
Arabidopsis [16] are beginning to make clearer the
mechanisms that regulate nitrogen assimilation. A better
understanding of the processes that occur in nitrogen
assimilation will enable plants to be produced that have a
high nitrogen use efficiency. Also by improving our
knowledge of mechanisms that play a part in the allocation
7 APS402 Dissertation
of nitrogen to seeds we could create a more nutritious
plant for consumption.
When looking at amino acid catabolism in humans our
knowledge is still very patchy [6], but with continued
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Candidate no: 000125738
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