Download An ecophysiological approach to modelling resource fluxes in

Journal of Experimental Botany, Vol. 50, No. 330, pp. 15–28, January 1999
An ecophysiological approach to modelling resource
fluxes in competing plants
Gilles Lemaire1,3 and Peter Millard2
1 INRA Station d’Ecophysiologie, F-86600 Lusignan, France
2 The Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
Received 10 May 1998; Accepted 17 August 1998
Abstract
Introduction
A conceptual model of resource acquisition and allocation within a generalized, individual plant growing
vegetatively in competition with others is presented.
The model considers C and N acquisition, synthesis of
assimilates and their transport and partitioning,
growth of new tissues, reserve formation and recycling, and losses due to root exudation and respiration.
These processes are regulated by the relative size of
the C and N substrate pools in shoot and roots, in
relation to meristematic sink strength. Translocation
and allocation patterns are represented according to
the Minchin phloem transport model. The current
model is used to consider the impact of competition
on resource acquisition and allocation, first by considering a plant growing in isolation and its response
to manipulation of light, CO and N supplies. Secondly,
2
competitive plants are introduced and the direct
effects on plant responses in terms of resource depletion are considered separately from indirect effects
such as potential changes in the quality of resources
available (e.g. light quality or soil N sources). In the
past, many studies of plant competition have not
established the importance of these indirect effects
because they have not established all the processes
involved in competition. This model can be used to
interpret responses of whole plants to their neighbours
in terms of the relative importance of both the direct
and indirect effects of competition.
Competition can be defined as the interactions between
individual plants induced by the necessity to share limited
resources, leading to a reduction of the number of survivors and/or a diminution of their growth (Begon et al.,
1986). To analyse the effect of plant competition on
resource fluxes it is, therefore, necessary to (i) consider
resource acquisition and use by individual plants in the
absence of competition (isolated plant model ); (ii) use
this model to analyse the response of individual plants to
a restriction in the availability of resources, as induced
by the presence of neighbouring plants; (iii) study how
the modification of the spatial distribution of the different
physical resources are governed by the presence of neighbouring plants, and how individual plants can perceive
these changes and develop an integrated response;
(iv) analyse the extent to which a plant can perceive the
presence of neighbouring plants by signals other than the
quantitative depletion of physical resources; and (v) integrate resource effects with non-resource effects in a more
comprehensive model at the level of the plant stand. Such
an ecophysiological approach deals with both intraspecific and inter-specific competition. In developing a
conceptual model there is no reason to think that changing
the neighbouring species should change anything in the
model, if the intrinsic capacities of the given species in
modifying the physical resources quantitatively and qualitatively are properly described and accounted for at the
scale of the individual plant.
The first section of this paper describes a mechanistic,
conceptual model for C and N partitioning in an isolated
plant and analyses how a plant develops integrated
responses to modifications in the availability of these
resources. The second section uses this isolated plant
model to analyse the overall response of an individual
Key words: C and N allocation, source-sink relations, conceptual model, whole-plant ecophysiology,
competition.
3 To whom correspondence should be addressed. Fax: +33 5 49 55 60 68.
© Oxford University Press 1999
16
Lemaire and Millard
plant to competition from neighbouring plants, as
observed in competition experiments. This paper will
focus mainly on the links between below- and aboveground resource fluxes and restrict ourselves to considering only C and N for the sake of simplicity and
clarity.
C and N fluxes in an isolated plant and their
regulation by the physical environment
Figure 1 represents the C and N fluxes between an isolated
plant and its environment and within the plant as a result
of the regulation of the different metabolic processes
leading to growth of the plant. These processes are
considered to be (1) carbon and nitrogen uptake and
assimilation, (2) transport and partitioning of assimilates,
(3) respiration, (4) use of assimilates for new tissue
formation, (5) storage of C and N, and (6) root exudation. For simplicity and clarity, water relations have not
been mentioned explicitly because water is not considered
as a resource used for plant growth, but as a resource
which affects the acquisition and the partitioning of N
and C by the plant. Therefore, the model assumes that
the plant does not experience any restriction in water
supply. Finally, only vegetative growth is considered, to
avoid the introduction of detailed mechanisms of reproductive development, which could differ greatly between
species. This simplification can be accepted if it is considered that competition for resources is directly linked to
the vegetative development of plants, even in situations
where the consequences of competition on reproductive
development of plants is also an important feature of
plant communities.
C and N substrate
The photoassimilates produced in leaves (sugars) constitute the C substrates, while the N substrate pool is
provided by the soluble reduced N produced either in
leaves or roots, depending on the chemical form of
external N (NO−, NH+, dissolved organic N, or N 3
4
2
fixation) and the localization of the nitrate reductase
activity ( leaf and/or roots). The substrate pool could be
defined as the quantity of C and N soluble compounds
which are readily available for any use, in any plant
tissue, and located in the cytosol. Thus the soluble C and
N compounds sequestrated in vacuoles or in organelles
like amyloplasts or chloroplasts are not considered as
part of the substrate pool. The estimation of the size of
the C and N substrate pools at the scale of the entire
plant is very difficult, but the relative concentration of
these two substrates in the different plant tissues plays an
important role in the transport and allocation of C and
N from source organs to the different sinks. C and N
substrates are transported in phloem from leaves to sink
organs by mass flow according to the Münch hypothesis
(Minchin et al., 1993; Sheehy et al., 1995), the driving
force being the difference in concentration in C plus N
substrates between the source and sink generating the
difference in osmotic potential. Both C and N substrates
are transported by the same mass flow, but at a rate
which is proportional to their relative concentration in
the source (Sheehy et al., 1996). Thus sucrose concentration in sources and sinks plays an important role in
substrate partitioning, as postulated by Farrar and Gunn
(1996). However, the local availability of C and N
substrates resulting from activity of source leaves, and
activity of different sinks along the transport path which
consume C and N substrates in variable proportions,
could also regulate partitioning. Thus the C:N ratio of
the substrate pool changes with time and varies between
the different organs of the plant. This may be an important
signal for the overall regulation of plant metabolism. C
substrates are generally not loaded into the xylem and
translocated up to shoot, but root exudates can represent
an important sink (Lambers, 1987) stimulating microbial
Fig. 1. Schematic representation of C and N fluxes within a vegetative plant growing in isolation. The diagram represents the plant as being
composed of three morphological components ( leaves, roots and stems). However, the model is not a compartmental representation of the plant.
Instead, the plant is split in three conceptual entities corresponding to the major plant functions: (i) metabolically active tissues responsible for
resource capture and assimilation of C and N substrate; (ii) supporting tissues allowing the plant to develop its architecture in relation to its
environment. (iii) storage tissues where C and N compounds are stored in specialized organelles. (1) C and N substrates (Csub — Ω and Nsub --- Ω)
represents, respectively, sucrose and reduced N circulating symplastically in the cytosol and transported from leaves to roots by the phloem massflow according to Münch hypothesis and the model of Minchin et al. (1993). N substrates move apoplastically in the xylem from the roots to the
shoots. Csub is provided directly from photosynthesis. The use of C for maintenance respiration is not represented on the diagram. Nsub is
provided by N uptake mechanisms (NO− and NH+ absorption and/or N fixation) and N assimilation processes either in roots or in leaves
3
4
2
depending on the main localization of the nitrate reductase activity. Nsub is constantly recirculating from roots to leaves through xylem water
stream. (2) Meristems and plant growth. Nsub and Csub are used in the leaf, stem and root meristems for new plant tissue formation. The rate at
which N and C are used in a meristem is under the control of its activity in terms of cell division rate, cell growth rate, and cell differentiation. A
part of Csub is directly used for growth respiration processes associated with new tissue synthesis but is not represented in the diagram. The overall
meristematic use of C and N can be represented by Michaelis-Menten equations according to Sheehy et al. (1996). The rate of C use in a meristem
is considered as led by N supply, it being the specific effect of N on cell division rate which determines sink-strength for C. Nsub sequestrated as
proteins in chloroplasts can be recycled and re-used as leaves age and senesce. (3) Reserve formation. Storage of proteins and starch or fructans
are regulated by numerous enzymes and requires transport of substrate across a membrane. These mechanisms are considered as highly inducible
by increased concentration of C and N substrates and for this reason their competition with meristematic sinks are considered as low. (4) Root
exudation. Csub and Nsub can be exuded from roots and used by rhizospheric microorganisms. By this way plants can affect soil N availability.
In the absence of any clear information on mechanisms involved in the control of exudation, only a positive feedback on Csub concentration in
root on C exudation flow is considered.
Modelling of resource fluxes
17
18
Lemaire and Millard
activity in the rhizosphere (Grayston et al., 1996). N
substrates can pass to the xylem and be transported up
to shoot with the flow of nitrate and reduced N (Simpson
et al., 1982; Oscarson and Larsson, 1986).
C and N supply
C substrates are produced by photosynthesis. The accumulation of sucrose in leaves represses the expression of
several photosynthetic genes (Sheen, 1990). Therefore,
the C supply of the plant is down-regulated by the
accumulation of C substrates. The photosynthetic activity
of the leaf is directly related to the amount of proteins
involved in the photosynthetic machinery used for light
harvesting and CO reduction. Rubisco is the most abund2
ant soluble protein in the leaves of C plants (Millard,
3
1988) and there is often a correlation between leaf photosynthesis in saturating light and the N or Rubisco concentration of leaves ( Evans, 1989). Maintenance respiration
can be considered as an unavoidable consumption of C,
being temperature dependent in shoots and roots and
proportional to the mass of proteins due to the energy
lost by protein turnover (Penning de Vries, 1975).
Therefore, the quantity of C substrate which becomes
available to the shoot and is used in shoot sinks or
translocated to the roots is the difference between plant
photosynthesis and shoot maintenance respiration. The
quantity of C substrate used for growth in root sinks is
equal to the daily flux of C substrate to root, minus the
daily roots respiration and loss of C as exudates. The
reduction of nitrate and assimilation of ammonium in
roots requires the use of C substrates as energy and
carbon skeletons. In leaves, a part of the energy can be
provided directly by photosynthesis (Beevers and
Hageman, 1980). The phloem translocation of amino
acids to roots could act as a signal for the down-regulation
of nitrate ( Tourraine et al., 1994), and also probably
ammonium absorption, through a direct repression of
specific ion transport. It has been shown that in trees the
rate of N uptake by roots is inversely proportional to the
concentrations of some amino acids in root phloem tissue
(Gessler et al., 1998). The best fit was achieved for
glutamic acid and glutamine while asparagine and other
nitrogenous constituents of the phloem sap of spruce
trees did not correlate with rates of N uptake. For N 2
fixation, the nitrogenase activity also seems to be downregulated by N substrates in the roots, through an effect
on the O diffusion barrier of the nodule (Oti-Boateng
2
et al., 1994). In contrast, mineral N absorption or N 2
fixation seem to be up-regulated by the flow of current C
assimilates in the roots, as shown by phloem girdling
experiments on trees (Goutouly, 1995), defoliation of
grasses (Clement et al., 1978) or lucerne ( Kim et al.,
1991) and by manipulation of CO assimilation rates of
2
plants through variation in the light level or CO concen2
tration (Gastal and Saugier, 1989). N -fixation by legumes
2
also seems to be regulated by the level of C supply in
both lucerne (Boller and Heichel, 1983; Vance et al.,
1979) and in white clover (Ryle et al., 1986). So the C5N
ratio of the substrate pool in roots appears to be a key
signal which allows the plant to regulate N uptake in
relation to the relative use of C and N substrates by the
different sinks.
C and N use in meristems
The activity of each meristem in a plant can be considered
as being regulated by factors such as apical dominance
and dormancy which lead to ontogenic plant morphogenesis. Plant morphogenesis can be considered as the expansion of a plant in space, with a specific shape resulting
from the initiation of meristems and their co-ordinated
activity. From the large variation of morphology between
species and individuals growing in the same environment
it is obvious that plant morphogenesis is genetically
programmed. Nevertheless, large phenotypic variations
occur with environmental changes, indicating that environmental signals and/or physical resources can affect the
expression of plant morphogenesis, perhaps due in part
to modification of the C and N resources shared between
the different meristematic sinks within the plant.
The sink activity of a single meristem can be considered
as resulting from production of new cells (cell division
rate), cell growth (cell expansion rate) and cell differentiation. The two former mechanisms determine the expansion rate of plant tissues, while the latter determines the
final weight per unit volume of the mature tissue produced
by the meristem (e.g. weight of C and N per unit of
volume). Thus, meristematic activity can be analysed as
a sequential use of C and N substrates for, successively,
cell division, expansion and differentiation mechanisms.
The rate of respiration of the meristematic tissues are
very high ( Zamski, 1996) because cell division requires
replication of DNA and protein synthesis. The consumption of sucrose by respiration of meristems has been
postulated to sustain the gradient between the phloem
and the sink cells (Geiger and Fondy, 1980) and a positive
relationship has been found between respiration rate and
root growth ( Kallarackal and Milburn, 1985). According
to Vertregt and Penning de Vries (1987), the energy costs
of the synthesis of a plant tissue can be related to the C
content of the tissue when mature, according to the
biochemical nature of the synthesized compounds. So the
estimation of the C requirement for the synthesis of a
new volume of plant tissue (the C demand of the sink)
can be estimated by the weight per unit volume of tissue
in the mature organs (Durand et al., 1991). It is therefore
possible to define the potential C demand of a given
meristematic sink as the C flux necessary to support the
rate of tissue expansion resulting from both the potential
Modelling of resource fluxes
cell division and cell expansion rates as determined by
genotypic and environmental factors such as temperature.
Farrar and Gunn (1996) suggested that sucrose concentrations in sinks positively affect the expression of genes
involved in growth, but increased C substrate concentrations only turn on the relevant genes if other factors such
as N and P supply or temperature are not limiting.
Increasing the temperature of meristems should increase
the potential for cell division, expansion and differentiation thereby increasing the potential rate of C flux
necessary to meet the sink demand and allow the expression of genes involved in these processes. As a consequence of any increase in potential sink activity, the
concentration of substrates in the cells tends to be
depressed and the rate of phloem unloading is stimulated.
In contrast, any decrease in sink activity will increase the
substrate concentration and so will depress the import of
C and N substrates.
The role of sucrose in the determination of sink strength
has often been emphasized because of its quantitative
importance as a substrate for respiration and as the main
contributor to osmotic regulation in phloem unloading.
Little attention has been given to the specific role of N
substrates in meristematic sink activity. Gastal and Nelson
(1994) showed that in the basal, elongating zone of grass
leaves, the rate of deposition of reduced N is mainly
associated with cell division, while Schnyder and Nelson
(1987) showed that deposition of C substrates is mainly
associated with cell expansion and cell differentiation.
Therefore, there is a spatial and temporal succession in
N and C substrate use by leaf meristems. There is also a
similar situation in growing root tips ( F Gastal, personal
communication). Therefore, the rate of N substrate flux
would first determine the rate at which DNA and proteins
can be replicated for cell division which, in turn, determines the further C substrate demand for subsequent cell
expansion and differentiation processes as a consequence
of the number of divided cells. Thus, not only should the
concentration of sucrose in the sink play an important
role in regulating sink activity, but also the relative
concentrations of C and N substrates. Because phloem
unloading in meristematic sinks is considered exclusively
to be a symplastic pathway ( Turgeon, 1987; Zamski,
1996), the C5N of substrate flux to a meristem sink is
that found in the phloem. A decrease in N substrate
concentration in the phloem, resulting from a low plant
N nutrition, will decrease the sucrose consumption in the
meristem as a consequence of a rapid decrease in the rate
of cell division, with only small effects on cell expansion
rate (Gastal and Nelson, 1994). This will lead to an
increased concentration of sucrose which, in turn, will
depress the phloem unloading rate. In contrast, an
increased N concentration in the phloem will promote
the rate of C use in meristematic sinks by increasing the
number of growing cells.
19
It is necessary to analyse separately the use of N in
photosynthetic tissues ( leaves) and in non-photosynthetic
tissues (roots and stems) and the consequences upon C
and N fluxes. The differentiation of photosynthetic cells
in leaf parenchyma requires N compounds for the formation of chloroplasts. This differentiation and the associated synthesis of proteins is largely induced by light
(Prioul et al., 1980). Gastal and Nelson (1994) showed
that the start of Rubisco synthesis in grass leaves occurred
after cell elongation was complete, with the maximum
rate of synthesis occurring at the emergence of the leaf
out of the sheath of the preceding leaf. These authors
also showed Rubisco formation in a leaf segment occurred
without new N deposition, suggesting that synthesis of
photosynthetic proteins is supported by N already in the
leaf, with an internal recycling of N compounds which
have already been used for cell division and early cell
elongation. Such recycling could occur during the differentiation of the different leaf tissues, from cells which
differentiate into vascular and supporting tissues to those
which differentiate into chlorophyllous parenchyma tissues. Thus Gastal and Nelson (1994) therefore showed
that with optimum nutrition the N concentration in leaf
tissues falls from about 8% in the zone of cell division to
about 4.5% in the mature leaf, this decrease being totally
explained by C accumulation with a constant pool of N.
In contrast, in roots, Gastal (personal communication)
showed that the N% in root tissues fell from a similar
initial value of 8% in root tips (cell division) to 2% in
mature root tissues. In this case, the accumulation of C
cannot account for all the observed decrease in %N.
Therefore N may be released and reused for further cell
division at the root tip. In consequence, root growth
appears less dependent than leaf growth on N supply.
Storage
Most plants store C and N. There are several possible
ecological advantages of storage which are important in
considering competition between plants. These are
(1) allowing growth to occur when the external availability of N is low, which can be important for perennial
species (Nambiar and Fife, 1991; Millard and Proe,
1993), particularly if there is a short growing season such
as in tundra ecosystems (Bloom et al., 1985), (2) to
enable more rapid recovery from catastrophic events such
as defoliation ( Thornton et al., 1994) and (3) to support
reproduction, for example, in species exhibiting monocarpic senescence (Millard, 1988). Furthermore, the efficient internal cycling of C and N within a plant through
the processes of storage and remobilization minimizes the
loss of resources from the individual (e.g. through leaf
litter), which would then only be available again in
competition with other plants and soil microbes.
Storage occurs if N or C can be ‘remobilized from one
20
Lemaire and Millard
tissue and subsequently used for the growth or maintenance of another’ (Millard, 1988). For the purpose of the
model two kinds of storage are considered, recycling and
reserve formation. Recycling occurs as a consequence of
tissue development or turnover (e.g. as a consequence of
protein turnover during senescence). Storage resulting in
recycling of resources, therefore, usually involves pools
which are metabolically active. An example of storage of
N by recycling is the case of Rubisco as a storage protein
(Millard, 1988). There are several ways in which N is
recycled from Rubisco. First, N can be recycled in the
canopy of both herbaceous and woody plants in relation
to the level of irradiance upon the leaves (Field, 1983;
Hirose et al., 1988; De Jong et al., 1989), thereby maximizing C assimilation. Secondly, N can be stored in coniferous trees as Rubisco and to a lesser extent chlorophyl
binding protein during the winter, and remobilized during
a flush of growth in spring to provide substrates for the
developing needles (Camm, 1993). While such spring
remobilization of N results in a decline in the photosynthetic capacity of mature needles (Camm, 1993), it is not
intimately linked to leaf senescence because the needles
may still function for a number of years (depending upon
the species). Thirdly, N is remobilized from Rubisco as a
consequence of leaf senescence in most species (Peeters
and Van Laere, 1994; Millard, 1996). Recycling of N can
also occur as a consequence of root turnover (e.g. after
defoliation of grasses or as found in the spring in young
trees).
Reserve formation differs from recycling in that it
involves N or C deposition in a discrete storage organelle,
such as a vacuole (Raven, 1987) or amyloplast (Zamski,
1996). Alternatively, reserve formation can utilize discrete
protein bodies as found in the seeds of many species
( Higgins, 1984) or the ray parenchyma cells of deciduous
trees (Sauter and Neumann, 1994). Reserve formation,
therefore, requires active transport of C or N across a
membrane. Resource allocation to reserve formation in
Fig. 1, therefore, will only occur when the other metabolic
sinks (e.g. meristems and respiration) have been satisfied.
This would explain why reserve formation tends to occur
only at times when the growth rate of the plant is low
(e.g. in the autumn) or when the external availability of
N or C is high in relation to the demands for growth. In
this way the plant can remove substrates from the cytosolic substrate pools and so avoid down-regulation of
either C or N uptake and assimilation.
Root exudates
The final sink for N and C substrates in the plant to
be considered is the secretion of root exudates.
Rhizodeposition of compounds, due to both root turnover
and release of organic compounds, constitutes a major
input of carbon into the soil. Estimates of the amount of
carbon entering soil through rhizodeposition vary, but
can be as great as 40% of the C assimilated by the plant
( Van Veen et al., 1991), with annual plants releasing less
of their fixed carbon than perennials. Despite being a
small proportion of the total rhizodeposition, exudates
are important in providing readily available substrates
for the growth of soil microbes. The composition of root
exudates has been well documented, and in addition to
reducing sugars, phenolic and organic acids also include
N-containing compounds such as amino acids and amides
(Grayston et al., 1996). The release of these compounds
from roots results in an enhanced microbial activity in
the rhizosphere compared with the bulk soil (Lynch and
Whipps, 1990). In turn, the soil microbes have a key role
in regulating N availability to the plant through the
processes of mineralization and nitrification. Exudation
can be both an active secretion of compounds and a
passive leakage along a concentration gradient (Grayston
et al., 1996). Our model suggests that the rate of exudation
would be controlled by the relative availability of C and
N substrates in the root substrate pool ( Fig. 1). C-replete
plants whose growth is N-limited have an increased
allocation of C to roots and a greater rate of exudation
of C substrates compared to plants grown with a
C-limitation. This, in turn, will lead to an increase in the
activity of soil microbes (which are themselves C-limited )
and so an increased potential for N uptake availability
in the soil.
Plant response to modification of its environment
The conceptual model represented in Fig. 1 can be used
for analysing the response of an individual plant to
changes in the availability of resources resulting from the
presence of competing plants. However, the effect of any
modification of C and/or N resources needs to be analysed
in terms of the requirement for both of these resources.
The effect of a change in the supply of one resource first
depends upon whether this resource is limiting or not for
plant growth. Therefore, before analysing the response of
plants to changes in the supply of resources, an examination will be made of how the plant acquires supplemental
C and N resources or uses C and N reserves in response
to changes in its growth as determined by temperature.
C and N supply and partitioning as affected by
temperature
An increase in temperature leads, in general, to an increase
in the activity of all meristems in a plant through a
response in the rate of cell division (Francis and Barlow,
1988) and a co-ordinated response of cell expansion rate
(Ben-Haj-Salah and Tardieu, 1995). The response of
meristems to increasing temperature is under the control
of N substrates, through their direct effect on cell division.
Modelling of resource fluxes
Therefore it is possible to describe the activity of a
meristematic sink by the rate of utilization of N substrates
using Michaelis–Menten kinetics, where the maximum
rate of substrate N use is a function of temperature
(Sheehy et al., 1996). The rate of C substrate use in a
meristem should, therefore, be driven by temperature and
N substrate concentration. So the C and N demand of
the meristems is increased by an increase in temperature,
creating greater competition among sinks within the plant
because the photosynthesis of source leaves and the N
uptake by roots does not respond to the same extent to
the change in temperature. For example, leaf elongation
rate of grasses can be increased 400% by an increase in
temperature from 10 °C to 25 °C (Gastal et al., 1992),
while leaf photosynthesis is only increased by 50% (Gastal
and Sangier, 1986). Warming a single meristem leads to
a rapid decrease in its cytosolic sucrose pool and so to
an increase in import of C and N substrates from phloem,
while cooling creates the reverse (Farrar and Gunn,
1996). As a consequence, source leaves accumulate carbohydrates within a few hours when roots are cooled
( Farrar, 1988). At the whole plant level, warming in the
short term creates a rapid increase of consumption of
substrates in both root and shoot meristems that is not
accompanied by a similar increase in C supply, because
of the less sensitive response of photosynthesis to temperature and the increase in maintenance respiration. As a
consequence of this discrepancy between C supply and
demand, the root meristems receive a decreasing proportion of the photoassimilates, due to the longer translocation pathway and the higher resistance to phloem flow,
as predicted by the model of Minchin et al. (1993). This
short-term effect of temperature on C partitioning
between roots and shoot has been confirmed by experiments with 14C labelling (Preud’homme et al., 1993). This
temperature effect gradually disappears in the long term
because (i) increasing leaf growth allows for more light
interception and so tends to restore the ratio between C
supply/C demand to the value prevailing before the
change in temperature, and (ii) some temporal modifications of the synthesis or hydrolysis of C reserves induced
by changes in sucrose concentration, can buffer the shortterm effect of temperature change (Farrar and Gunn,
1996). Thus, in an environment where resources are not
limited, an isolated plant tends to restore its ontogenic
partitioning of C and N after any change in temperature,
even if a short-term modification of C allocation can be
observed as a consequence of a temporary discrepancy
between C supply and demand. This view is supported
by the fact that the accumulation of sucrose stimulates
the formation of reserves through the expression of genes
involved in starch and fructan synthesis (Farrar and
Gunn, 1996). So decreasing the temperature leads to a
higher proportion of C stored in reserves, through an
21
increase in concentration of sucrose as a consequence of
a decreased meristematic activity.
Modifications of C supply
Any decrease of C supply leads to a rapid proportional
decrease in the N uptake rate, whatever the form of N
utilized. Inversely, an increase in C supply leads to a
proportional increase in N uptake, but as shown by
Gastal and Saugier (1989), this proportionality between
C and N supplies cannot be maintained above a given
threshold value of C supply rate. In such conditions of
high C supply, the N uptake capacity of a plant is no
longer limited by the C substrate concentration in roots,
but by the negative feedback due to recycling of N
substrates in the phloem.
The main consequence of variations in the C supply to
the plant is a modification of C partitioning. Any reduction in C supply, whatever the cause, leads to a higher
proportion of assimilated C allocated to shoot growth at
the expense to roots, with the reverse observed with
increasing C supply (Ryle and Powell, 1976; Gastal and
Saugier, 1986). These general observations can be analysed with the help of Fig. 1. According to the assimilate
transport model of Minchin et al. (1993), it can be
considered that the total resistance pathway from source
to sink is less from leaf sources to shoot sinks than to
root sinks, any reduction in C substrate concentration in
source leaves should induce a greater proportion of C
substrate flow in the lower resistance pathway. The reverse
should also occur with increases in C substrate concentrations in the source leading to proportionally more C flow
through the highest resistance pathway, i.e. to the roots.
This explains why increasing the irradiance of a plant can
result in a greater allocation of carbon to roots and an
increased loss of C as exudates (Hodge et al., 1997). The
higher resistance for phloem transport to root meristems
compared to shoot meristems can be linked to the distance, but also to the existence of a greater number of
anatomical connections between the different phloem
sieve tubes. Therefore, the anatomical architecture of the
phloem imposes a kind of priority rule for shoot meristems against root meristems for C allocation. This priority
rule allows the plant to have a more rapid restoration of
C supply by favouring a more rapid expansion of leaf
area and light capture, allowing a subsequent increase of
C allocation to roots, as the C economy of the plants
improves.
Figure 1 suggests that the effect of manipulation of C
supply on shoot/root C allocation depends mainly on the
level of C demand resulting from the total potential
meristematic activity of the whole plant. If C supply
exceeds demand, a reduction of C supply should not
affect shoot/root growth, until a threshold value is reached
where it equals C demand. Any further decrease in C
22
Lemaire and Millard
supply will then lead to the expression of the ‘shoot
priority’ and as a consequence to an increase in
shoot5root ratio. Therefore, the effect of any manipulation in C supply on the shoot5root ratio has to be
analysed in terms of C supply5C demand ratio, and not
in terms of C supply only. In this way it is possible to
explain many contradictions in the literature on the effect
of elevated CO on shoot/root growth (Farrar and Gunn,
2
1996). The predictions of our model agree with the
concept of a functional equilibrium between shoot and
root developed by Brouwer (1963).
The other way to examine C partitioning within the
plant is to consider allocation to meristems versus reserve
formation. Figure 1 shows that an increase in C substrate
concentration in source leaves increases both C fluxes to
meristems and to reserve formation. There is little evidence in the literature on the priority between these two
fluxes. However, most observations of whole plants show
that shoot meristem activity saturates before reserve
formation increases, when the C supply is increased.
Inversely, shoot growth remains unaffected when there is
a paucity of C and demand exceeds the supply, because
C reserves can be used directly to support meristematic
activity. Therefore, the effects of manipulation of C supply
on growth versus reserve C partitioning also has to be
analysed in terms of C supply:C demand ratio and not
in terms of the absolute C supply.
Modifications of N supply
N deficiency leads to an increase in C substrate concentration in source leaves which, according to the model of
Fig. 1, results in an increasing proportion of C being
allocated to root growth (Belanger et al., 1992). The
effect of manipulation of N supply has to be analysed in
relation to the ratio between C supply and demand. If
the plant is in a situation of excess C supply relative to
demand, any decrease in N supply will not affect C
partitioning between root and shoot meristems, and any
increase in N supply will not affect C partitioning either,
until the C demand becomes higher than the C supply.
One of the important responses of a plant to a restriction in N supply is the trade-off between leaf growth and
leaf N concentration. With a limited N supply what is
the optimum response for the plant in terms of C economy? Two options exist, either maximizing leaf meristematic activity, leaf extension rate and interception of
light while minimizing leaf N concentration and photosynthetic capacity per unit leaf area, or the reverse. Grindlay
(1997) suggested that not all species have the same
balance between these two responses. Maximizing leaf
growth should tend to give plants a greater competitive
ability, but at the expense of a longer-term investment of
C in leaf meristems, while maximizing leaf N concentration should give an immediate C gain. The optimum
between these two responses should be dependent on the
response of leaf photosynthesis to leaf N concentration
and should, therefore, be different between C and C
3
4
species because the optimum leaf N concentration for
photosynthesis is lower in C species.
4
C and N partitioning for balanced growth
Co-ordination between root and shoot growth has been
reported by many authors as a consequence of a ‘functional equilibrium’ (Brouwer, 1963; Davidson, 1969).
This concept considers the plant as composed of only
two functional compartments, shoot and roots, which are
involved in C and N acquisition, respectively. The model
in Fig. 1 allows the identification of four plant compartments: leaf and root tissues which are directly involved
in C and N acquisition, the supporting tissues (e.g. stems)
and storage tissues. All compartments in total result in
the architecture of the plant as a whole and its adaptation
to the constraints of its environment. Körner (1991)
showed that for a large range of species of the same
alpine habitat, the partitioning of dry matter between
shoot and root was often resulting from the partitioning
between stems and storage root and not between leaves
and fine roots (Fig. 2). In the same way, Allirand et al.
(1992) showed that the change in shoot5root ratio of
lucerne plants with temperature was only the consequence
of a change in stem5tap root ratio while the leaf5fine
root ratio remained constant. Stem growth is mainly
associated with structural tissue formation, while tap root
growth contributes to reserve formation. Thus, the
shoot5root ratio only reflects the functional equilibrium
of young, annual plants with shoots composed mainly of
photosynthetic leaf tissues and with predominantly fine
roots. Even considering the leaf compartment alone, a
greater proportion of supporting tissues was required in
sorghum as the size of the leaf lamina increased (Lemaire
and Gastal, 1997). The study of C and N partitioning
within a plant has to move from a morphological point
of view to a more functional viewpoint. As proposed by
Caloin and Yu (1984) and developed further by
Greenwood et al. (1991) herbaceous plants can be considered as having both metabolic and structural compartments. The metabolic compartment represents the plant
mass directly associated with C and N acquisition
( leaves+fine roots) and directly associated with growth,
while the structural compartment represents the plant
mass not directly involved in plant growth processes, such
as storage or supporting tissues. A similar approach has
been taken in modelling C allocation of trees, using the
pipe model theory of Shinozaki et al. (1964) to relate C
allocation between organs with tree architecture (Beringer
and Nikinmaa, 1997). Thus, the growth rate of a freestanding plant can be considered as proportional to the
size of its metabolic compartment and, as shown by
Modelling of resource fluxes
23
Fig. 3. Relationship between shoot plant N% and shoot plant mass
( W ) for individual plants of Sorghum bicolor growing in isolation (&)
or in a dense crop (O, 6, %, corresponding to three successive dates
of sampling). The continuous line represents the equation N%=
5.06( W )−0.11 for isolated plants. The dotted line represents the equation
N%=7.79( W )−0.34 for the average plant of the dense crop (crop shoot
mass divided by plant density) (after Lemaire and Gastal, 1997).
C and N partitioning in plants in response to
competition by neighbouring plants
The consequences of competition by neighbouring plants
for C and N partitioning can be studied at two levels of
organization, either at the level of the plant stand, referring to the functioning of a hypothetical ‘average plant’,
or at the level of each of the individual plants by
considering the hierarchical relationship for light interception between individuals within the canopy.
Fig. 2. The partitioning of dry matter in different plant species (redrawn
)
from Körner, 1991). ( e ) leaves; ( % ) stems; ( & ) storage roots; (
fine roots.
Caloin and Yu (1982) for Dactylis glomerata and by
Lemaire and Gastal (1997) for Sorghum bicolor and
Medicago sativa, the plant metabolic weight increases as
(total plant weight)a with a value of a close to 0.80–0.85.
This indicates that structural mass increases in a relatively
higher proportion than total plant weight as the plant
grows. As a consequence, if we consider that the ‘metabolic’ compartment of the plant consists primarily of the
photosynthetic machinery (with a high N concentration),
and that the ‘structural’ compartment consists mainly of
cell walls and carbohydrate reserves, this allometry
between these two plant compartments leads to a decrease
in plant N% with increasing plant mass, as illustrated in
Fig. 3. Therefore, the study of the allocation pattern of
C and N within plants must account for size and stage
of development of the plant size. The effects of similar
environmental constraints on shoot5root or leaf5stem C
or/and N allocation will not have the same effect when
comparing plants of different sizes, whatever the cause of
these differences.
From an isolated plant to the average plant in dense stand
The rapid decline in plant N% observed at canopy level
when competition for light occurs seems to be mainly the
consequence of a decline in leaf area ratio (LAR) of
plants, resulting from a higher investment in structural
and supporting tissues with low N content, at the expense
of metabolic tissues with a high N concentration in leaves
(Greenwood et al., 1990; Gastal and Lemaire, 1997). So
as the size of the plant increases, a greater proportion of
these non-metabolic tissues are necessary to support and
connect an increasing quantity of metabolic tissues ( leaves
and roots). Competition inside a dense canopy results in
‘isometric’ growth of the average plants. This leads to a
greater investment in supporting tissues than for an
isolated plant of the same size, allowing the leaves of the
competing plant to be placed at the top layer of the
canopy to reach light and so assimilate more C. Lemaire
et al. (1992) showed in lucerne stands that the decline in
leaf5stem ratio as the competition for light becomes more
intense was the driving phenomenon leading to the decline
in plant N%. As illustrated in Fig. 4, a straight line can
be drawn between the N content in shoots and the LAI
of a lucerne stand, despite that a progressively greater
24
Lemaire and Millard
Fig. 4. Accumulation of N in leaves (6, +) and in shoots
( leaves+stems: O, Ω) in relation with LAI during regrowth of lucerne
stand in spring (dark symbols) or in summer (open symbols).
proportion of the shoot N is invested in stem tissues,
thereby allowing the new leaves to emerge at the top of
the canopy.
It is not easy to take into account roots at the level of
the plant stand. It can only be expected that, as for
isolated plants, the growth of the metabolic root tissue
and the allocation of the associated C and N should
respond to changes in the environment in a way which is
co-ordinated with leaf area development, according to
the ‘functional equilibrium’. Therefore, as competition
for light increases in a dense canopy, and the C supply
to an average plant decreases, according to Fig. 1 a lower
proportion of C should be allocated to roots, in a similar
response to that of shading an isolated plant. Some
authors have reported such a progressive increase in
shoot5root ratio during canopy development of different
crops ( Troughton, 1977; Hanson et al., 1991). However,
for perennial species with storage tissues localized in
either stems (trunk) or tap roots, a similar functional
equilibrium response can lead to a different pattern of
resource allocation in morphological terms. Therefore,
the above-ground5below-ground or shoot5root ratios
have to be used with caution because they may have little
functional significance.
From an average plant to the individual plant in dense stand
Figure 3 shows that in dense stands, individual plants do
not necessarily follow the usual relationship between %N
and mass observed for the whole stand (or for an ‘average’
plant). When this relationship is observed for isolated
plants, the differences in plant mass due to plant–plant
variation at a given date, or the differences due to plant
growth between dates, gives a similar pattern of decline
in %N as discussed above, with smaller plants having
higher %N. However, when plants of different size are
compared in a dense canopy, the smaller plants which
experience stronger competition for light have a much
lower N% than predicted by their size, compared to the
dominant plants which have a %N closer to that of
isolated plants. Such observations have been confirmed
on a lucerne stand by Avice et al. (1997), who showed
that not only was the N concentration in the shoots of
plants reduced owing to their size, but that the reserve
formation of N in vegetative storage proteins was
restricted. Therefore, the partitioning of N to shoots can
be affected by the hierarchical position of plants inside
the canopy, as a consequence of an increased investment
in structural-supporting tissues, and the consequent
reduced N uptake capacity of the plant resulting in less
N reserve formation. These data can be interpreted using
the model of Fig. 1. Smaller plants in a dense stand have
a low C supply because they are shaded and have to
support an increasing demand for C to maximize the
growth of supporting shoot tissues. In addition, the lack
of C substrate in roots could also restrict the ability of
plants to take up nutrients from soil.
Shading effect: light quantity and light quality
The causes of the modification of plant morphology and
of the associated C and N allocation pattern between
metabolic and structural compartments resulting from
competition for light are not well understood. The reason
is that it is difficult to separate properly the direct effect
of shading, linked to the decrease in light quantity and C
supply, from the indirect effects due to the photomorphogenetic responses of plants to the changes in light
quality, due to differential extinction of red and far red
light within the canopy. One important adaptive feature
to shade is the photosynthetic acclimation in response to
a change in irradiance, which allows the plant to minimize
the reduction of its C supply (Pearcy and Sims, 1994).
Many studies (Aphalo and Ballaré, 1995) have demonstrated that most plants are able to change their morphology and their allocation pattern of C in response to
changes in light quality by means of photoreceptors
sensitive either to the red5far red ratio (phytochromes)
or to blue light (cryptochromes). Two types of morphological adaptation can be considered according to the
species. For some plants the change in light quality leads
to shade tolerance responses, characterized by an increase
in leaf area ratio and specific leaf area (Bourdot et al.,
1984; Peace and Grubb, 1982). In other species, the
perception of low red:far red ratios triggers several morphological responses, such as increased stem internode
elongation, reduced leaf5stem dry weight ratio and
increased shoot5root dry weight ratio (Ballaré et al.,
1991; Aphalo and Letho, 1997) and can be considered as
a shade avoidance response. Shade avoidance responses
results in the plant allocating an increasing proportion of
Modelling of resource fluxes
25
its C to support shoot tissues. Kasperbauer et al. (1984)
showed that root growth of Glycine max (L.) was
depressed by end-of-day far red treatment. Using similar
treatments, Robin et al. (1992) showed that photomorphogenetic responses of white clover plants led to an
increasing proportion of assimilated 14C being used for
growth of petiole and stolon internodes, to the detriment
of root growth. So the decrease in red5far red ratio
associated with shading in a plant canopy should emphasize the direct effect of the diminution of C supply. Our
model (Fig. 1) predicts that a reduced C supply should
lead to a reduced proportion of C allocated to root
growth. In clover, the photomorphogenetic response to a
change in light quality will increase the proportion of C
allocated to the growth of structural shoot tissues associated with ‘light foraging’ and so decrease the C available
for root growth.
Another important morphological response of plants
to a decrease in red:far red ratio is a reduction in tillering
or branching (Deregibus et al., 1985). If new tillers or
branches are considered as a replication of the main
morphological unit at a younger ontogenic stage, branching can be postulated as being an optimum way for the
colonization of the horizontal space, by younger and,
therefore, smaller morphological units with a high LAR.
The inhibition of branching and tillering by shading, and
the preferential allocation of C to the main shoot meristems corresponds to a change from a predominantly
horizontal to a more vertical strategy of growth, leading
to a rapid decrease in plant LAR. Gautier and VarletGrancher (1996) and Gautier et al. (1997), showed that
the decrease in blue light associated with shading provokes
morphological responses in white clover plants, allowing
the leaves to be positioned higher in the canopy. Plants
also perceive their neighbours through the horizontal
reflection of far red light allowing a response to competition before the quantity of light intercepted by the plant
is reduced (Ballaré et al., 1987). Part of the hierarchy
developed between individual plants inside a stand of
vegetation for light capture and, therefore, for acquisition
of soil resources could be the result of the responses
developed during the early stage of canopy development,
and the sensitivity of their perception of the presence of
neighbouring plants.
Experiments with split root systems have demonstrated
clearly that the uptake capacity per unit root length could
be increased up to 3-, and sometimes 10-fold when a part
of the roots were deprived of nutrients. Burns (1990)
showed that the fraction of the root system experiencing
nutrient deprivation influences the extent to which uptake
rates increase elsewhere, so the uptake rate at the whole
plant level could be maintained, as predicted by the
overall control of N uptake by N and C substrate
concentration in roots (see Section I ).
Many authors have reported a high proliferation of
roots in nutrient rich patches ( Fitter, 1994). This observation could be considered as contradictory to our model
( Fig. 1) where allocation of C to roots is considered to
be restricted with increasing plant N nutrition. But, as
described by Fitter (1994), the changes of root architecture by means of a local proliferation of fine root branching at the expense of elongation of a large diameter root
axis, does not necessarily require any supplementary C.
Moreover, Robinson (1994) pointed out that local proliferation of fine roots in nutrient rich patches is often
accompanied by a restriction of root growth elsewhere.
So plasticity of root architecture may be expressed only
within the limit imposed by the allocation of C to root
meristems, resulting from the control of partitioning at
the level of the whole plant. Recently, Zhang and Forde
(1998) have identified a gene involved in lateral root
proliferation and shown gene expression to be triggered
by nitrate. So local NO− concentration could be consid3
ered as a qualitative signal for plants in determining the
plasticity of their root growth. The sensitivity of different
species to such a signal could, therefore, explain the
variation in response in root growth between species to
nutrient patches as observed by Grime (1994). Since
nitrate is a very mobile ion in soil solutions such root
proliferation might not be very important in regulating
nitrate uptake. However, such a response could have a
large effect on the ability of a plant to take up less mobile
ions such as phosphate (Robinson, 1996). Further studies
are necessary to determine the extent to which nutrient
patches could be created from and maintained by means
of rhizosphere C flow and the subsequent effects on
rhizosphere microorganisms (Stark, 1994).
Responses to soil heterogeneity
Conclusion
The distribution of mineral resources in soils are very
heterogeneous, at scales ranging from centimetres to
metres. This heterogeneity can be experienced by the root
system of individual plants (Stark, 1994; Caldwell, 1994).
Heterogeneity of soil nutrient resources in soil can affect
plant nutrient uptake in two ways: (i) a local modification
of nutrient absorption rate per unit of root tissue, and/or
(ii) a local modification of root growth and root architecture (Robinson, 1994).
The conceptual model that has been developed here is
based upon the representation of the plant as the sum of
the three functional components: (i) the plant tissue
involved directly in resource capture, (ii) structural plant
tissue associated with plant architecture, and (iii) storage.
The internal communication between these different components is by phloem transport of assimilates, which
allows the allocation of C and N substrates from leaf
sources to the different sinks. Down-regulation of C and
26
Lemaire and Millard
N uptake and of the assimilation processes by the internal
concentration of C and N in substrate pools plays an
important role for the control of C and N acquisition by
a whole plant. The role of reserve formation in controlling
internal C/N concentration of substrate has been emphasized. The model of source/sink partitioning developed by
Minchin et al. (1993) allows the prediction of a priority
for C and N use by leaf meristems as C supply is reduced
relatively to C demand, and the model predicts qualitatively many observed responses of plants to manipulations
of C and N resources.
Balanced C and N supply for plant growth has to be
analysed according to the increasing proportion of structural tissue of low N content as the plant grows, leading
to a decline of N requirement per unit of C gain. In a
dense stand, competing plants have to increase their
investment in structural tissues in order to reach light.
For this reason it can be hypothesized that within a
population of competing plants, N acquisition from the
soil by individual plants should be related to their hierarchical position for light interception within the canopy.
Plant responses to qualitative signals, such as changes
in red5far red ratio or local variation in soil NO−
3
concentration, to develop their shoot and root architecture for optimizing resource capture should play an
important role in determining the competitive ability of
the individual within the population.
Acknowledgement
The authors are grateful to the Scottish Office Agriculture,
Environment and Fisheries Department for the grant they
provided G Lemaire to fund this work.
References
Allirand JM, Gosse G, Lemaire G. 1992. Influence of temperature on lucerne dry matter and nitrogen distribution. In:
Scaife A, ed. Proceedings of the 2nd Congress of the European
Society of Agronomy, Warwick, 24–25.
Aphalo PJ, Ballaré CL. 1995. On the importance of information
acquiring systems in plant–plant interactions. Functional
Ecology 9, 5–14.
Aphalo PJ, Letho T. 1997. Effects of light quality on growth
and N accumulation in birch seedlings. Tree Physiology
17, 125–132.
Avice JC, Ourry A, Lemaire G, Volenec JJ, Boucaud J. 1997.
Alfalfa intraspecific competition and the involvment of
reserve availability. Crop Science (in press).
Ballaré CL, Sanchez RA, Scopel AL, Casal JJ. 1987. Early
detection of neighbour plants by phytochrome perception of
spectral changes in reflected sunlight. Plant, Cell and
Environment 10, 551–557.
Ballaré CL, Scopel AL, Sanchez RA. 1991. Photocontrol of
stem elongation in plant neighbourhoods: effects of photon
fluence rate under natural conditions of radiation. Plant, Cell
and Environment 14, 57–65.
Beevers L, Hageman RH. 1980. Nitrate and nitrite reduction.
In: Stumpf PK, Conn EE, eds. The biochemistry of plants,
Vol. 5, 115–168.
Begon M, Harper JL, Townsend CR. 1986. Ecology, individuals,
populations and communities. Oxford: Blackwell.
Belanger G, Gastal F, Warembourg F. 1992. The effect of
nitrogen fertilisation and the growing season on carbon
partitioning in a sward of tall fescue. Annals of Botany
72, 401–408.
Ben-Haj-Salah M, Tardieu F. 1995. Temperature affects expansion rate of maize leaves without change in spatial distribution
of cell length. Plant Physiology 109, 861–70.
Beringer F, Nikinmaa E. 1997. Implications of varying pipe
model relationships on Scots Pine growth in different climates.
Functional Ecology 11, 146–156.
Bloom AJ, Chapin III FS, Mooney HA. 1985. Resource
limitation in plants—an economic analogy. Annual Review of
Ecological Systems 16, 363–392.
Boller BC, Heichel GH. 1983. Photosynthate partitioning in
relation to N -fixation capacity of alfalfa. Crop Science
2
23, 655–659.
Bourdot GW, Saville DJ, Field RJ. 1984. The response of
Achilea millefolium L. (yarrow) to shading. New Phytologist
97, 653–663.
Brouwer R. 1963. Some aspects of the equilibrium between
underground and overground plant parts. Jaarbocke, Institute
voor Biologische en Scheikunding, Wageningen 213, 31–34.
Burns IG. 1990. Influence of the spatial distribution of nitrate
on the uptake of N by plants: a review and a model for
rooting depth. Journal of Soil Science 31, 155–173.
Caldwell MM. 1994. Exploiting nutrients in fertile soil microsites. In: Caldwell M, Pearcy RW, eds. Exploitation of
environmental heterogeneity by plants. Ecological processes
above- and below-ground. San Diego: Academic Press,
325–347.
Caloin M, Yu O. 1982. An extension of the logistic model of
plant growth. Annals of Botany 43, 599–607.
Caloin M, Yu O. 1984. Analysis of the time-course change in
nitrogen content of Dactylis glomerata L. using a model of
plant growth. Annals of Botany 54, 69–76.
Camm E. 1993. Photosynthetic response in developing year-old
Douglas-fir needles during new shoot growth. Trees 8, 61–66.
Clement CR, Hopper MJ, Jones LPH, Leafe EL. 1978. The
uptake of nitrate by Lolium perenne from flowing nutrient
solution. II. Effect of light, defoliation, and relationship to
CO flux. Journal of Experimental Botany 29, 1173–1183.
2
Davidson RL. 1969. Effect of root/leaf temperature differentials
on root/shoot ratios in some pasture grasses and clover.
Annals of Botany 33, 561–569.
De Jong TM, Day KR, Johnson RS. 1989. Partitioning of leaf
nitrogen with respect to within canopy light exposure and
nitrogen availability in peach (Prunus persica). Trees 3, 89–95.
Deregibus VA, Sanchez RA, Casal JJ, Trlica MJ. 1985. Tillering
responses to enrichment of red light beneath the canopy in a
humid natural grassland. Journal of Applied Ecology 22,
199–206.
Durand JL, Varlet-Grancher C, Lemaire G, Gastal F, Moulia B.
1991. Carbon partitioning in forage crops. Acta biotheoretica
39, 213–224.
Evans JR. 1989. Photosynthesis and nitrogen relationships in
leaves of C plants. Oecologia 78, 9–19.
3
Farrar JF. 1988. Temperature and the partitioning of translocated carbon. In: Long SP, Woodward FI, eds. Plants and
temperature. Cambridge University Press, 203–235.
Farrar JF, Gunn S. 1996. Effects of temperature and atmospheric
carbon dioxide on source-sink relations in the context
of climate change. In: Zamski E, Schaffer AA, eds.
Modelling of resource fluxes
Photoassimilate distribution in plants and crops; source-sink
relationships. New York: Marcel Dekker, 389–406.
Field C. 1983. Allocating leaf nitrogen for the maximization of
carbon gain: leaf age as control on the allocation program.
Oecologia 56, 341–347.
Fitter AH. 1994. Architecture and biomass allocation as
components of the plastic response of root systems to soil
heterogeneity. In: Caldwell MM, Pearcy RW, eds.
Exploitation of environmental heterogeneity by plants.
Ecophysiological processes above- and below-ground. San
Diego: Academic Press, 305–324.
Francis D, Barlow PW. 1988. Temperature and the cell cycle.
In: Long SP, Woodward FI, eds. Plants and temperature.
Cambridge: Company of Biologists Ltd, 181–202.
Gastal F, Belanger G, Lemaire G. 1992. A model of leaf
extension rate of tall fescue in response to nitrogen and
temperature. Annals of Botany 70, 437–442.
Gastal F, Lemaire G. 1997. Nutrition azotée et croissance des
peuplements végétaux cultivés. In: Morot-Gaudry JF, ed.
Assimilation de l’azote chez les plantes. Aspects physiologiques,
biochimiques et moleculaire. INRA-Editions, Serie ‘Mieux
Comprendre’, 355–367.
Gastal F, Nelson CJ. 1994. Nitrogen use within the growing
leaf blade of tall fescue. Plant Physiology 105, 191–197.
Gastal F, Saugier B. 1986. Alimentation azotee et croissance de
la fetuque elevee. I. Assimilation du carbone et repartition
entre organes. Agronomie 6, 157–166.
Gastal F, Saugier B. 1989. Relationships between nitrogen
uptake and carbon assimilation in whole plants of tall fescue.
Plant, Cell and Environment 12, 407–418.
Gautier H, Varlet-Grancher C. 1996. Regulation of leaf growth
of grass by blue light. Physiologia Plantarum 98, 424–430.
Gautier H, Varlet-Grancher C, Baudry N. 1997. Effects of blue
light on the vertical colonization of space by white clover
and their consequences for dry matter distribution. Annals of
Botany 80, 665–671.
Geiger DR, Fondy BR. 1980. Phloem loading and unloading:
pathways and mechanisms. In: Fritz GL, ed. What’s new in
plant physiology, Vol. 11. Florida: Gainesville University,
25–28.
Gessler A, Schreider S, von Sengbush D, Weber P, Haneman U,
Huber Ch, Rothe A, Kreutzer K, Rennenberg H. 1998. Field
and laboratory experiments on the uptake of nitrate and
ammonium by the roots of spruce (Picea abies) and beech
(Fagus sylvatica) trees. New Phytologist 138, 275–285.
Goutouly JI. 1995. Regulation de l’absorption de NO− chez le
3
pêcher. Etude en solution nutritive. Thèse de Doctorat.
Institut National Polytechnique de Lorraine, Nancy (France).
Grayston SJ, Vaughan D, Jones D. 1996. Rhizosphere carbon
flow in trees, in comparison with annual plants: the
importance of root exudation and its impact on microbial
activity and nutrient availability. Applied Soil Ecology
5, 29–56.
Greenwood DJ, Gastal F, Lemaire G, Draycott A, Millard P,
Neeteson JJ. 1991. Growth rate and%N of field grown crops:
theory and experiments. Annals of Botany 67, 181–191.
Greenwood DJ, Lemaire G, Gosse G, Cruz P, Draycott A,
Neeteson JJ. 1990. Decline in percentage N of C and C
3
4
crops with increasing plant mass. Annals of Botany 66,
425–436.
Grime JP. 1994. The role of plasticity in exploiting environmental heterogeneity. In: Caldwell MM, Pearcy RW, eds.
Exploitation of environmental heterogeneity by plants.
Ecophysiological processes above- and below-ground. San
Diego: Academic Press, 1–19.
27
Grindlay DJC. 1997. Towards an explanation of crop nitrogen
demand based on optimization of leaf nitrogen per unit leaf
area. Journal of Agricultural Science, Cambridge 128, 377–396.
Hanson AC, Andren O, Steen E. 1991. Root production of
four arable crops in Sweden and its effect on abundance of
soil organisms. In: Atkinson D, ed. Plant root growth,
an ecological perspective. Oxford: Blackwell Scientific
Publications, 247–266.
Higgins TVJ. 1984. Synthesis and regulation of major proteins
in seeds. Annual Review of Plant Physiology 35, 191–221.
Hirose T, Werger MJA, Pons TL, Van Rheenen JWA. 1988.
Canopy structure and leaf nitrogen distribution in a stand of
Lysimachia vulgaris L., as influenced by stand density.
Oecologia 77, 145–130.
Hodge A, Paterson E, Thornton B, Millard P, Killham K. 1997.
Effects of photon flux density on carbon partitioning and
rhizosphere carbon flow of Lolium perenne. Journal of
Experimental Botany 48, 1797–1805.
Kallarackal J, Milburn JA. 1985. Respiration and phloem
translocation in roots of chickpea. Annals of Botany 56,
211–218.
Kasperbauer MJ, Hunt PG, Sojka RE. 1984. Photosynthate
partitioning and nodule formation in soybean plants that
received red or far-red light at the end of the photosynthetic
period. Physiologia Plantarum 61, 549–554.
Kim TH, Ourry A, Boucaud J, Lemaire G. 1991. Changes in
source–sink relationship for nitrogen during regrowth of
lucerne following removal of shoots. Australian Journal of
Plant Physiology 18, 593–602.
Korner Ch. 1991. Some often overlooked plant characteristics
as determinants of plant growth—a reconsideration.
Functional Ecology 5, 162–173.
Lambers H. 1987. Growth, respiration, exudation and symbiotic
association: the fate of carbon translocated to the roots. In:
Gregory PJ, Lake JV, Rose DA, eds. Root development and
functions. Cambridge University Press.
Lemaire G, Gastal F. 1997. N uptake and distribution in plant
canopies. In: Lemaire G, ed. Diagnosis of nitrogen status in
crops. Heidelberg: Springer-Verlag.
Lemaire G, Khaity M, Onillon B, Allirand J.M, Chartier M,
Gosse G. 1992. Dynamics of accumulation and partitioning
of N in leaves, stems, and roots of lucerne (Medicago sativa
L.) in a dense canopy. Annals of Botany 70, 429–435.
Lynch JM, Whipps JM. 1990. Substrate flow in the rhizosphere.
Plant and Soil 129, 1–10.
Millard P. 1988. The accumulation and storage of nitrogen by
herbaceous plants. Plant, Cell and Environment 11, 1–8.
Millard P. 1996. Ecophysiology of the internal cycling of
nitrogen for tree growth. Journal of Plant Nutrition and Soil
Science 159, 1–10.
Millard P, Proe MF. 1993. Nitrogen uptake, partitioning and
internal cycling in Picea sitchensis (Bong.) Carr. as influenced
by nitrogen supply. New Phytologist 125, 113–119.
Minchin PEH, Thorpe MR, Farrar JF. 1993. A simple
mechanistic model of phloem transport which explains sink
priority. Journal of Experimental Botany 44, 947–955.
Nambiar EKS, Fife DN. 1991. Nutrient retranslocation in
temperate conifers. Tree Physiology 9, 185–207.
Oscarson P, Larsson CM. 1986. Relations between uptake and
utilization of NO− in Pisum growing experimentally under a
3
nitrogen limitation. Physiologia Plantarum 67, 109–117.
Oti-boateng C, Wallace W, Sisbury JH. 1994. The effect of the
accumulation of carbohydrate and organic nitrogen on N
2
fixation (acetylene reduction) of faba bean cv. Fiord. Annals
of Botany 73, 143–149.
28
Lemaire and Millard
Peace WJH, Grubb PJ. 1989. Interaction of light and mineral
nutrient supply on the growth of Impatiens parviflora. New
Phytologist 90, 127–150.
Pearcy RW, Sims DA. 1994. Photosynthetic acclimation to
changing light environments; scaling from leaf to whole plant.
In: Caldwell MM, Pearcy RW, eds. Exploitation of environmental heterogeneity by plants. Ecophysiological processes
above-and below-ground. San Diego: Academic Press, 175–208.
Peeters KMU, van Laere AJ. 1994. Amino acid metabolism
associated with N-mobilization from the flag leaf of wheat
(Triticum aestivum L.) during grain development. Plant, Cell
and Environment 17, 131–141.
Penning de Vries FWT. 1975. The cost and maintenance
processes in plant cells. Annals of Botany 39, 77–92.
Preud’homme M, Gastal F, Belanger G, Boucaud J. 1993.
Temperature effects on partitioning of 14C assimilates in tall
fescue (Festuca arrundinacea Schreb.). New Phytologist 123,
255–261.
Prioul JL, Brangeon J, Reyss A. 1980. Interaction between
external and internal conditions in the development of
photosynthetic features in a grass leaf. I. Regional responses
along a leaf during and after low-light or high-light
acclimation. Plant Physiology 66, 762–769.
Raven JA. 1987. The role of vacuoles. New Phytologist
106, 357–422.
Robin C, Varlet-Grancher C, Gastal F, Flenet F, Guckert A.
1992. Photomorphogenesis of white clover (Trifolium repens
L.) phytochrome-mediated effects on 14C-assimilate partitioning. European Journal of Agronomy 1, 235–240.
Robinson D. 1994. The response of plants to non-uniform
supplies of nutrients. New Phytologist 127, 635–674.
Robinson D. 1996. Resource capture by localized root proliferation: why do plants bother? Annals of Botany 77, 179–185.
Ryle GJA, Powell CE. 1976. Effect of rate of photosynthesis
on the pattern of assimilate distribution in the graminaceous
plants. Journal of Experimental Botany 27, 189–199.
Ryle GJA, Powell CE, Gordon AJ. 1986. Defoliation in white
clover: nodule metabolism, nodule growth and maintenance,
and nitrogenase functioning during growth and regrowth.
Annals of Botany 57, 263–271.
Sauter JJ, Neuman V. 1994. The accumulation of storage
materials in ray cells of poplar wood (Populus×canadensis
‘robusta’): effect of ringing and defoliation. Journal of Plant
Physiology 143, 21–26.
Schnyder H, Nelson CJ. 1987. Growth rate and carbohydrates
fluxes within the elongation zone of tall fescue blades. Plant
Physiology 85, 548–553.
Sheehy JE, Mitchell PL, Durand JL, Gastal F, Woodward FI.
1995. Calculation of translocation coefficients from phloem
anatomy for use in crop models. Annals of Botany 76, 263–269.
Sheehy JE, Gastal F, Mitchell PL, Durand JL, Lemaire G,
Woodward FI. 1996. A nitrogen-led model of grass growth.
Annals of Botany 77, 165–177.
Sheen J. 1990. Metabolic repression of transcription in higher
plants. The Plant Cell 2, 1027–1038.
Shinozaki K, Yoda K, Hozumi K, Kira T. 1964. A quantitative
theory of plant form—the pipe model theory. I. Basic
analysis. Japanese Journal of Ecology 14, 97–105.
Simpson RJ, Lambers H, Dalling MJ. 1982. Translocation of
nitrogen in a vegetative wheat plant (Triticum aestibum).
Physiologia Plantarum 56, 11–17.
Stark JM. 1994. Causes of soil nutrient heterogeneity at
different scale. In: Caldwell MM, Pearcy RW, eds.
Exploitation of environmental heterogeneity by plants.
Ecophysiological processes above- and below-ground. San
Diego: Academic Press, 225–284.
Thornton B, Millard P, Duff EI. 1994. Effects of nitrogen supply
on the source of nitrogen used for regrowth of laminae after
defoliation of four grass species. New Phytologist 128,
615–620.
Tourraine B, Clarkson DT, Muller B. 1994. Regulation of
nitrate uptake at the whole plant level. In: Roy J, Garnier E,
eds. A whole plant perspective on carbon-nitrogen interactions.
The Hague: SPB Academic Publishing, 11–30.
Troughton A. 1977. The rate of growth and partitioning of
assimilates in young grass plants: a mathematical model.
Annals of Botany 41, 553–565.
Turgeon R. 1987. Phloem unloading in tobacco sink leaves:
insensitivity to anoxia indicates a symplastic pathway. Planta
171, 73–83.
Vance CP, Heichel GH, Barnes DK, Bryan SW, Johnson LE.
1979. Nitrogen fixation, nodule development, and vegetative
regrowth of alfalfa (Medicago sativa L.) following harvest.
Plant Physiology 64, 1–8.
Van Veen JA, Liljeroth G, Lekkerkerk LJA, Vande Geijn SC.
1991. Carbon fluxes in plant–soil systems at elevated
atmospheric CO levels. Ecological Applications 1, 175–181.
2
Vertregt N, Penning de Vries FWT. 1987. A rapid method for
determining the efficiency of biosynthesis of plant biomass.
Journal of Theoretical Biology 128, 109–119.
Zamski E. 1996. Anatomical and physiological characteristics
of sink cells. In: Photoassimilate distribution in plants crops:
source–sink relationships. New York: Marcel Dekker, Inc.
283–310.
Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene
that controls nutrient-induced changes in root architecture.
Science 279, 407–409.