Modelling Nutrition

Scientia Horticulturae 74 1998.
4782
Modelling plant nutrition of horticultural crops:

a review
J. Le Bot ) , S. Adamowicz 1, P. Robin
INRA, Unite de Recherche en Ecophysiologie et Horticulture, Domaine St. Paul, Site Agroparc,
84914 Aignon, Cedex 9, France
Accepted 19 September 1997
Abstract
In this review, studies in plant nutrition are classified according to their time scales and microor macroscopic level of approach. Short-time scale studies are mostly dealt by plant physiologists
with the prospect of building mechanistic models. They describe elementary plant functions
implicated in, or dependent on ion uptake, with the goal of explaining the mechanisms underneath
the functions. The concept of active ion transport across the root plasma membrane derives from
precise analyses of uptake isotherms describing nutrition as a function of ion concentration in the
root medium. Attempts to introduce feedback mechanisms, as required to model whole-plant
response to the environment, are reviewed. Similarly, the response of plant photosynthetic
capacity to leaf nitrogen status is extremely rapid and the role of nitrogen in regulating
photosynthesis seems to hold for a large number of species. Therefore, it appears possible to
introduce nitrogen regulation on leaf photosynthesis, thus allowing better simulations of plant
growth under nitrogen limiting conditions. Long-time scale studies are dealt by agronomists and
have long been the basis of fertilization advice. They attempt to predict crops mineral nutrient
requirements over the entire cycle from the empirical knowledge of general laws governing crop
growth. Recent advances propose to manage nutrition on the basis of crop structure independently
from species and give opportunities to develop mechanistic concepts at this time scale. For
nitrogen, this has been formalized extensively in crops such as cereals and grasses. It deserves to
be carefully looked at for horticultural crops. These models also provide a sound basis to diagnosis
through plant analysis. In horticultural agrosystems, such as those found for hydroponic cultures
under commercial glasshouses, the use of on-line sensors is currently an alternative to crop
models, since fertilization is induced by the immediate response of the sensors. This practice made
Corresponding author. E-mail: lebot@avignon.inra.fr

E-mail: adamow@avignon.inra.fr
2
E-mail: robin@avignon.inra.fr
1
0304-4238r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved.

PII S 0 3 0 4 - 4 2 3 8 9 8 . 0 0 0 8 2 - X
J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782
48
possible by technological breakthrough is meant to correct drifts but lacks anticipation. q 1998
Elsevier Science B.V.
Keywords: Efflux; Functional equilibrium; Influx; Mineral ions; Model; Nitrogen; Photosynthesis; Plant
growth; Regulation; Uptake rates
Contents
1. Introduction .
...............................................
48
2. Proximate functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1. Nutrient uptake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.1. Influx isotherms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.2. Efflux measurements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.3. Net uptake isotherms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2. Feedback regulation of uptake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.1. Influx . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.2. Efflux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.3. Net uptake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3. Nutrient use efficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.1. Nutrients and photosynthesis: a casual relationship? . . . . . . . . . . . . . . . . . . . .
2.3.2. Several models . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.3. Nutrients and water fluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.3.1. Is there a casual relationship between PNUE or mineral concentrations and
WUE? Is mineral uptake, in particular nitrogen, controlled by plant water fluxes? . . . .
52
52
53
54
55
56
57
58
59
59
59
61
62
3. Ultimate functions . . . . . . . . . . . . . . . .
3.1. Nutrient uptake and functional equilibrium .
3.2. Growth control by nutrients . . . . . . . . .
3.3. Growth demand of nutrients . . . . . . . . .
3.3.1. Statistic approach . . . . . . . . . .
3.3.2. Mechanistic approach . . . . . . . .
.
.
.
.
.
.
64
64
65
66
66
67
...................
...................
...................
69
69
70
...............................................
73
..................................................
75
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
4. Operational approach of nutrition . . . . . . . . . . . . . . . . .

4.1. Diagnostic of nutritional status . . . . . . . . . . . . . . . .
4.2. Managing the cultural system: the greenhouse as an example
5. Conclusions .
References
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
63
1. Introduction
Plants acquire from their aerial and root environments all constituents of their tissues.
In particular, soil fertility governs plant growth and thereby the quantities of mineral
nutrients taken up by the roots. In natural ecosystems, the minerals absorbed by growing
organisms return to the soil after organic matter decomposition, and soil fertility is more
or less maintained through nutrient cycling. In cultivated ecosystems, however, all
49
harvested biomass withdrawn from the field contains nutrients that no longer return to
the soil. Hence, maintenance of soil fertility and plant yield production depend of
counterbalancing fertilizer inputs. Considering all the nations in the world, grain yield
increases linearly with the doses of N q P q K. fertilizers applied to cereals and this
accounts for more than 80% of the variance in yield Greenwood, 1990.. From the
viewpoint of agricultural productivity, it means that mineral nutrition is the main factor
limiting growth and therefore high fertilizer inputs are necessary to produce large
quantities of biomass. This idea explains the peculiarity of horticulture where fertilization is extremely intensive: although nitrate concentration in the soil solution of a fertile
field ranges between 2 to 20 mol my3 Mengel and Kirkby, 1987; p. 365., the nutrient
solution used to grow tomatoes in soilless cultures is maintained in between 1525 mol
my3 NOy
3 . Meanwhile, 1 ha of fertile wheat field yielding 8 tonnes of grains produces
around 14 tonnes of aerial dry biomass, whereas 1 ha of greenhouse yielding 450 tonnes
of tomatoes produces around 40 tonnes of total aerial dry biomass.
Since the XIXth century, it is well known that plant growth is always limited by the
first factor whose availability in the environment starts missing. This fundamental
concept has guided research to render modern agriculture more efficient. The contemporary research in crop physiology has identified the factors limiting plant growth Table
1., tempted to delay their upcoming limitation or change their order of appearance, and
quantified their potential productivity increase when economically profitable.
These lines of research resulted in increasingly more complex models of plant growth
processes and yields which offer today the operational bases for strategic long-term.
and tactical short-term. crop management. Meanwhile, industrialization and breakthrough in technology have given growers powerful and sophisticated tools to manipulate these factors. Moreover, for highly profitable potential productivity increases, new
agrosystems have been developed to manipulate the naturally fixed limiting factors. For
instance, the development of horticulture in protected environments proceeds from this
technical breakthrough and growers use in their greenhouses CO 2 enrichment, soilless
cultural techniques, artificial lighting and heating and cooling to increase productivity.
It may seem a paradox to trace the first reports on plant water and mineral nutrition
back to the XVIIth century and state that today there is still controversy about the
mechanisms of ion uptake, and moreover, the use of mineral nutrition in crop models
Fig. 1 ; Table 2..
Table 1
Factors limiting plant yield. For non-fixed factors, the names expensive and cheap refer to the cost in energy
required to set-up the desired factor modified after Mohr and Schopfer, 1995.
Fixed factors
CO 2 concentration
Light integral
Temperature
Type of soil
Non-fixed factors
Expensive factors
Cheap factors
Irrigation
Fertilization
Crop protection
Nutritional value
Plant density
Time of sowing
Genotype
External yield quality
50
Fig. 1. Different approaches for modelling the uptake of a nutrient wXx. All numbers refer to models listed in
Table 2. The direction of the arrows indicate which factor is explained target. by an explicative factor.
Dashed lines refer to regulatory processes.
Agronomists and plant physiologists have developed a dual approach to characterize

the uptake of a mineral nutrient wXx by a plant. A mechanistic approach describes
uptake as successive steps: uptake per se i.e. the entrance of wXx inside the root.,
assimilation if any. andror transport in the plant and at last utilisation in plant
metabolism Fig. 1; groups 1, 2 and 3.. Research along these lines aims at explaining the
proximate factors controlling mineral uptake. Hence, modelling is set at fine spatiotemporal scales: short-time studies at the cellular and molecular levels. The uppermost
important question concerns the identification of uptake regulatory processes likely to
happen in one or several successive steps. In the end, only the integration of these
successive steps will simulate adequately the behaviour of a whole plant. The second
statistic approach has anteriority and proceeds from higher levels of integration. This
research focus on the ultimate factors governing the equilibrium between mineral
uptake and plant demand considered through growth Fig. 1; groups 4 and 5.. From this
viewpoint, modelling is set at a broad spatio-temporal scale: long-time studies months,
year. at the whole plant or field levels. This approach has resulted in the actual
fertilization practices, which attempt simultaneously to maintain soil fertility by a
maintenance fertilization. and to fulfil the crop-growth demand by a growth
fertilization.. Table 2 is a non-exhaustive compilation of the authors which have
developed the main concepts used as starting points for models dealing with plant
mineral nutrition.
This review will concentrate on the main models of plant mineral nutrition published
in the literature with an attempt to explicate the hypotheses underneath the concepts. It
reflects our view of agronomists seeking for a leading thread in the plentiful literature on
plant nutrition. Thereby, we have tried here to organize the current hypotheses into a
logical conceptual frame suitable for whole-plant physiologists and agricultural engi-
Table 2
A brief history of plant nutrition modelling. In the model column, s. and m. refer to statistic and mechanistic models. The group column refers to the place of the
models in Fig. 1
Explicative factors
Model
Growth: final yield
dose of one element

dose of one element
plant nutrient content
dose of two or more elements
dynamic
Nutrient
content: KqCaqMg
N
N
N
Uptake
rate:
K, Na, Cl,
SO4 , NO 3 ,
NH 4
K, Cl
NO 3
NO 3
NO 3
PO4
Group Authors
law of minimum s.
diminishing return s.
critical concentration s.
nutrient equilibrium s.
4
4
5
4
rate of supply of one element relative addition rate m.

plant N, P, K contents
critical concentration s.
4
5
thermodynamic activity ratio

total aerial biomass
plant compartments
plant compartments
solution ion content
MichaelisMenten m.
plant and solution contents

plant NO 3 content
plant NO 3 content
root respiration
root length
HqrOHy excretion NO 3 , NH 4 and

SO4 assimilation
Root respiration
anion uptake
Photosynthesis
specific leaf N
selectivity constant m.
diminishing N demand s.
2 compartments m.
core-skin m.
14
68
68
68
1
feedbackrMichaelis s.
pumpleakbuffer m.
feedbackrMichaelis s.
CN interaction m.
CN interaction s.
17
17
17
18
18
cytoplasmic pH-stat m.
1238
energy requirement m.
CN interaction s.
8
3
von Liebig 1841.

Mitscherlich 1909.
Ulrich 1952.
Homes
` and van Schoor 1982.
1992.; Larsson 1994.

Ingestad and Agren
Burns 1990.
Hansen 1972.; Nielsen and Hansen 1984.; Nielsen and Srensen 1984.
Greenwood et al. 1990.; Lemaire and Gastal 1997.
Caloin and Yu 1984.
Hardwick 1987.
Epstein 1972.
Siddiqi and Glass 1982.; Cram 1983.

Scaife 1989.
Buysse et al. 1996.
Le Bot 1991.; Andriolo 1995.
Sanders 1993.
Explained
factorrfunction
Dijkshoorn et al. 1968.; Ben Zioni et al. 1971.

Veen 1980.; Lambers et al. 1983.; van der Werf et al. 1988.
Sinclair and Horie 1989.
51
52
neers interested by the subject. The scheme of this paper is set on the description of the
dual spatio-temporal approach mentioned above, which is in our view the most
interesting for horticulture. For reasons of conciseness, we will not develop extensively
the role of each nutrient in plant metabolism, information on the implication of mineral
nutrition in crop production being reviewed elsewhere Le Bot et al., 1994.. At last, this
paper aims to unify different modelling approaches by exploring the diversity of species
and environments studied so far. This is a reason why we will not confine our analysis
to horticultural plants. Moreover, modelling in this field is too scarce to justify a
separate study from other agrosystems.
2. Proximate functions
2.1. Nutrient uptake
In productive agrosystems, ion concentration at the root surface level is determined
both by the properties of the rooting medium and by the plant ion uptake kinetics.
Clarkson 1985. reviewed these interface aspects between plant physiology and soil
science. For example, he reported on the work of Silberbush and Barber 1983.
showing that root elongation rate and soil diffusion coefficient are the main determinants
of phosphorus uptake rate by roots. Thus, although these aspects are not dealt with in
this paper, it is important to stress that the knowledge of nutrient distribution and
mobility in soils or substrates, as well as uptake capacity distribution and architecture of
roots for review, see Habib et al., 1991. are required to model nutrition. Furthermore,
these determine the root units that plant physiologists should prefer. However, although
for phosphorus most works relate uptake to root surface or length, for other nutrients
only more accessible units such as root dry or fresh weights are commonly used, which
may be a limit for models.
Plants regulate their tissue mineral composition against electrochemical gradients
through active and passive processes. This explains why mineral concentrations are
sometimes lower e.g. Ca, Na, and toxic elements. or higher e.g. N, P, S, K. in the
plant than in the soil solution. Extensive research on ion uptake has been dedicated to
characterizing plant ability to extract nutrients from the soil solution. In particular,
uptake velocity has been related to external nutrient concentration, thus, yielding the
so-called uptake isotherms, most of the time using young plants grown in well defined
environmental conditions or excised roots. While results have proven useful in defining
sound ecological properties of the transport systems, they are questionable in the context
of rich soil environments, typical of intensive horticultural systems. In fact, technical
difficulties seriously limit the accuracy of uptake rate measurements when the nutrient
concentration is elevated, and or. with older plants.
y
2y
2y .
For most ions Kq, Naq, Ca2q, Cly, NHq
, uptake is the net
4 , NO 3 , PO4 , SO4
result between simultaneous influx from the solution to the roots and efflux from the
roots to the solution, these processes being considered independent Clarkson, 1986;
Aslam et al., 1996a.. Many studies are concerned with net uptake or influx, but since
53
high values of efflux have been reported, it influences significantly net uptake and
should be considered in its regulation.
Influx of anions being mostly ATP-dependent, the existence of a significant amount
of efflux is puzzling, as it may be seen as an energy-wasting process. Indeed, due to
efflux, net anion uptake could require 25 to 100% more energy than expected from
theoretical values van der Werf et al., 1988; Bouma and De Visser, 1993.. As a
consequence, in addition to growth and biomass maintenance, Johnson 1990. proposed
two supplemental specific components for root respiration, one being the energy cost of
ion uptake and the other the energy cost of ion re-uptake i.e. the uptake needed to
balance efflux.. Some data also suggest that efflux occurs through specialized specific
systems requiring both RNA and protein synthesis Aslam et al., 1996a.. To date, the
physiological role of efflux, if any, is unclear. It might be an essential process, the most
direct way to regulate internal ion concentration Miller and Smith, 1996., and the
respiration re-uptake component would be the cost of homeostasis.
2.1.1. Influx isotherms
Influx kinetics are established by measuring the accumulation rate of an isotope e.g.
13
q
N or 15 N for nitrogen. or an analogue e.g. ClOy
for potassium. in
3 for nitrate, Rb
plant tissues. To minimize efflux, the shorter the experiments the better, experiments
shorter than 10 min being preferable Clarkson, 1986; Nissen, 1991.. However, due to
sensitivity limits, many published data were obtained over 30 min to 1 h periods, leading
to large influx rate underestimation.
q
q.
For low concentrations e.g. under 1 mol my3 for NOy
influx rate
3 , NH 4 or K
increases with ion concentration following an hyperbola. Since the early work of Epstein
and Hagen 1952., the mechanistic enzyme kinetic formula of Michaelis and Menten
Table 3 is widely accepted as best describing this behaviour. Two parameters, Im also
notated Vm . and K m also notated K or C0,5 . characterize this model. The former, the
maximal rate of influx, is a capacity parameter which can be approached at high external
concentrations. Its value is related both to the number of transporters per root unit and to
their intrinsic characteristics. The latter is the ion concentration mol my3 . for which
influx rate is half the maximum. The lower its value the higher is the affinity of the
transporter for a particular ion. It does not depend on the root units but it is determined
only by intrinsic characteristics of the transporter.
Table 3
Formulas used for ion influx I . into roots. Im , Im1 and Im2 maximum influx, K m , K m1 and K m2
MichaelisMenten constants, x s nutrient solution concentration of ion X
Formula
I s Im =
xs
xs q K m
xs
xs
I s Im1 =
q Im2 =
xs q K m
x s q K m2
xs
I s Im =
q b = xs
xs q K m
Type
Authors
MichaelisMenten
Epstein and Hagen 1952.
Dual MichaelisMenten
Epstein et al. 1963.
MichaelisMentenqLinear
Kochian and Lucas 1982.
54
If kinetic measurements are made at higher concentrations above 1 mol my3 for
q
q.
NOy
, influx rate increases again and reaches much higher values than
3 , NH 4 or K
predicted by Im . Such a complex pattern has been described for Kq, Naq, Cly, Mg 2q,
q
PO42y, SO42y, NOy

3 , NH 4 and most micro nutrients Berlier et al., 1969; Laties, 1969;
Epstein, 1972; Hodges, 1973; Nissen, 1974; Rao and Rains, 1976.. The molecular
interpretation of influx kinetics over a wide range of concentration has led to considerable debate Laties, 1969; Epstein, 1972; Hodges, 1973; Nissen, 1974, 1991; Borstlap,
1981; Smart et al., 1996., but the dual transport mechanism of Epstein 1972. is the
most widely accepted. Mechanism I or HATS for high affinity transport system.
operates in the low concentration range, obeys simple MichaelisMenten kinetics and
shows very low K m values. Reported K m and Im values are greatly variable with plant
age, species or varieties and growth conditions Glass and Siddiqi, 1984a; Clarkson,
1985; Schenk, 1996., but also due to resolution of the measurement set-up. For nitrate,
ammonium and potassium, most K m values lay between 5 and 100 = 10y3 mol my3
Glass and Siddiqi, 1984a; Peuke and Kaiser, 1996., but values as high as 985 = 10y3
mol my3 have also been reported for nitrate Pace and McClure, 1986.. Mechanism II
or LATS for low affinity transport system. operates mostly in the higher concentration
range and its kinetic is not clearly characterized. There are reports that influx rate fits the
saturable MichaelisMenten kinetics with lower affinity i.e. higher K m . and higher Im
than HATS Peuke and Kaiser, 1996.. Observed K m values for LATS reach 25 mol
my3 for nitrate Peuke and Kaiser, 1996. and 3 to 19 mol my3 for potassium Benlloch
et al., 1989; Maathuis and Sanders, 1996; Smart et al., 1996.. However, most published
q
2y
q
data on NOy
describe a linear influx in the high range of external
3 , NH 4 , PO4 , and K
ion concentration. According to Bieleski 1973. when experimental concentrations are
far below the K m value of LATS, a linear expression is an adequate approximation of a
MichaelisMenten hyperbola. Only one parameter characterizes the linear LATS kinetics i.e. the slope between uptake rate and nutrient concentration. and it should be
expressed in m3 hy1 per root unit. Reported values, in m3 hy1 gy1 of fresh root, range
from 150 = 10y6 Kronzucker et al., 1995a. to 14 = 10y3 Peuke and Kaiser, 1996. for
nitrate, from 670 = 10y6 to 1.3 = 10y3 Wang et al., 1993b. for ammonium, and from
160 = 10y6 Kochian and Lucas, 1982. to 540 = 10y6 Kochian et al., 1985. for
potassium.
Overall influx is usually computed as the sum of HATS and LATS components
Table 3., referring either to the dual MichaelisMenten kinetics with four parameters
two for maximum influx and two for affinity. or single MichaelisMenten plus a linear
component, with three parameters Im and K m of HATS, and slope of LATS..
2.1.2. Efflux measurements
The use of isotopes in influx studies allows the determination of efflux by monitoring
the accumulation of natural isotope originating from the roots. into the nutrient solution
Morgan et al., 1973.. As for influx, experiments should be as brief as possible but due
to low analytical sensitivity, nitrate efflux determinations for concentrations above 0.1
mol my3 last for about 1 h, thus resulting in underestimated values. To overcome this
problem, efflux is usually computed rather than measured, either by subtracting net
uptake from influx Deane-Drummond, 1986; Macduff and Jackson, 1992., or through
55
compartmental analysis Cram, 1968; Pitman, 1971; Devienne et al., 1994a. which may
appear too cumbersome a procedure. Therefore, little information is available on efflux
in the high concentration range, above 1 mol my3 for nitrate and ammonium Macklon
et al., 1990; Devienne et al., 1994b.. It should also be emphasized that efflux values
may be largely artefactual. Usually, experimental set-ups require the transfer of the
plants from their cultivation medium prior measurements. In some cases, the resulting
transplant shock has been shown to inhibit net uptake for several hours Bloom and
Sukrapanna, 1990., due to a dramatic enhancement of efflux, while influx remained
unchanged Delhon et al., 1995a; Aslam et al., 1996b..
Depending on growth conditions and species, efflux rates mol hy1 gy1 root fresh
weight. range from 4 = 10y9 Kronzucker et al., 1995b. to 10 = 10y6 for nitrate
Deane-Drummond and Glass, 1983., and from 100 = 10y9 to 4 = 10y6 for ammonium
Wang et al., 1993a.. Expressed in percentage of influx, efflux ranges from 5% Siddiqi
et al., 1991; Kronzucker et al., 1995b. to 93% Devienne et al., 1994b. for nitrate, from
910% Wang et al., 1993a; Kronzucker et al., 1995c. to 3335% Macklon et al.,
1990; Kronzucker et al., 1995c. for ammonium, and values of 30% have also been
reported for phosphate and sulphate Lee, 1993.. Efflux is mostly seen as an unidirectional leak, depending only on the root ion content, but independent of the external ion
concentration Breteler and Nissen, 1982; Mackown, 1987; Teyker et al., 1988..
2.1.3. Net uptake isotherms
Under near constant ion concentrations, net uptake is measured by the difference
between initial and final ion content in the nutrient medium. Some experimental set-ups
allow the continuous monitoring of ion concentrations and solution volume which are
maintained at set points through automatic additions Clement et al., 1974; Andre et al.,
1979; Blom-Zandstra and Lupijn, 1987; Alloush and Sanders, 1990; Freijsen et al.,
1990.. Plant ion and water uptake are computed as the added amounts. Depending on
the sensitivity of the experimental set-ups and ion concentrations, their time-scale ranges
from a few minutes to 3 h. Accumulation of an isotope in plant tissues during a long
time of exposure 1 h at least. can also be used as an estimate of net ion uptake
Macduff and Jackson, 1992; Ourry et al., 1996.. Uptake isotherms are usually obtained
under variable ion concentrations, following the depletion method of Claassen and
Barber 1974.. Plants are transferred to a small solution volume and are allowed to
deplete a particular ion until its concentration becomes constant. Manual or automatic
Goyal and Huffaker, 1986. ion titration allows to compute net uptake rate against ion
concentration. However, the time necessary to complete an experiment increases with
increasing initial ion concentrations, which seriously limits isotherm studies to a very
low range. Experiments may last for about 10 h for nitrate and phosphate at respective
initial concentrations of 250 = 10y3 mol my3 and 30 = 10y3 mol my3 and 4 h for
potassium at initial concentration of 200 = 10y3 mol my3 . However, since net uptake
shows diurnal variations even under constant ion concentrations, we believe that these
isotherms probably happen to be distorted.
Net uptake characteristics are mostly the same as those deduced from the influx
studies, i.e. existence of two uptake mechanisms, the first being saturable. The
MichaelisMenten kinetics have been adapted to take efflux into account Table 4..
56
Table 4
Formulas used for net ion uptake In. into roots
Formula
In s In m =
In s In m =
xs
yE
xs q K m
x s y x cp .
x s y x cp . q K m
Type
Authors
Influx minus efflux E .
Claassen and Barber 1974.
Compensation point x cp .
Nielsen 1976.
Claassen and Barber 1974. proposed a model where net uptake is the mere difference
between influx, following simple MichaelisMenten kinetics, and efflux, considered as
a constant. The model of Nielsen 1976. does not include efflux explicitly, but considers
that the ion concentration necessary for null net uptake, as measured at the end of
depletion experiments, is an ion compensation point. Both models are currently used to
fit the data, but in view of the stated mechanistic independence of influx and efflux
Clarkson, 1986; Aslam et al., 1996a., the formulation of Claassen and Barber should be
preferred.
2.2. Feedback regulation of uptake
Evidence has accumulated showing that uptake characteristics of both HATS and
LATS are not fixed values, but are closely dependent on experimental conditions and
plant growth demand. Under near constant ion concentrations, net uptake of nitrate
Clement et al., 1978; Tribo-Blondel,
1979; Pearson et al., 1981; Le Bot and Kirkby,
1992; Delhon et al., 1995a; Andriolo et al., 1996; Ourry et al., 1996., ammonium Wild
et al., 1987; Ourry et al., 1996. and potassium Wild et al., 1987; Le Bot and Kirkby,
1992; Macduff and Dhanoa, 1996; Ourry et al., 1996. undergo continuous variations, the
pattern being roughly. an increase during the light period and a decrease during the
night. For nitrate, these variations have been stated for concentrations as low as
20 = 10y3 mol my3 Ourry et al., 1996. and as high as 5 mol my3 Pearson et al.,
1981.. Nitrate and ammonium net uptake rates are strongly reduced by defoliation Wild
et al., 1987; Macduff and Jackson, 1992. in less than 90 min, and reduction in nitrate
uptake rate becomes significant within 20 min Wild et al., 1987.. These continuous and
rapid variations in uptake rates cannot be explained by changes in the root system size
or by synthesis of new transporters. In addition, different ions share common uptake
patterns in these experiments. For these reasons, it has been suggested that uptake rates
are controlled by a common, non-specific, mechanism, presumably transpiration or the
flow of carbon compounds from leaves to roots, necessary to the respiration-dependent
influx Wild et al., 1987.. Today, the former hypothesis is rejected see Section 2.3.
while the latter is not. However, as variations of uptake rate take place even when
nutrient concentration is limiting, the second hypothesis seems also unlikely. What is
more, homeostasis can hardly be explained by non-specific mechanisms, and underneath
most studies, regulation lays on negative feedback from internal specific components.
57
Given its relative importance and sensitivity to internal ion concentration, efflux
might explain both homeostasis and net ion uptake regulation Miller and Smith, 1996..
Since the early work of Morgan et al. 1973. introduced efflux as a regulatory
component of net nitrate uptake and Deane-Drummond and Glass 1983. suggested that
it might be the main short-term regulator, experimental results have led to contradictory
and much debated results. During the daynight cycle under constant ion concentrations,
net nitrate uptake variations have been stated to be due only to efflux Pearson et al.,
1981., or mostly to influx Delhon et al., 1995a.. In experiments involving nutritional
pre-treatments, net nitrate uptake regulation has also been explained by either efflux
Breteler and Nissen, 1982; Deane-Drummond and Glass, 1983; Mackown, 1987., influx
Lee and Drew, 1986; Lee, 1993. or both Teyker et al., 1988; Devienne et al., 1994b;
Kronzucker et al., 1995b.. While different results may be explained by specific
differences and experimental peculiarities, it remains that modelling both fluxes is a
necessity. Successful incorporation of nutrition dynamics in a crop model requires
correct and simultaneous simulation of homeostasis, energy cost and net uptake.
2.2.1. Influx
The simplest, most general and selective regulation mechanism lays on the sensitivity
of the transport systems to the internal concentration of the particular transported ion
Glass and Siddiqi, 1984a.. Indeed, inverse relationships between root non-metabolized.
ion concentration and influx rates have been stated for nitrate Siddiqi et al., 1990;
Delhon et al., 1995a., ammonium Wang et al., 1993b., sulphate Clarkson et al., 1983.,
phosphate Lefebvre and Glass, 1982., chloride Cram, 1983. and potassium Siddiqi
and Glass, 1987.. Most studies focused on the HATS, for which Im appears to be
inversely related to root ion concentration. K m has been found positively correlated to
root ion concentration for ammonium Wang et al., 1993b. and potassium Siddiqi and
Glass, 1987., or constant for sulphate Clarkson et al., 1983., while reports are
conflicting for nitrate Lee and Drew, 1986; Siddiqi et al., 1990.. For a linear LATS, it
has also been reported, both for ammonium Wang et al., 1993b. and nitrate Siddiqi et
al., 1990. that the slope parameter is lower when root ion concentration is high.
A model of root ion concentration negative feedback on HATS has been introduced
by Siddiqi and Glass 1982, 1986. for potassium uptake Table 5.. For this particular
ion, the relationships of Im and K m with root potassium concentration are exponential
with negative and positive parameters, respectively. Therefore, the original Im and K m
values of the MichaelisMenten model have been replaced by their statistical relationship with root potassium concentration so that Im and K m become, respectively, the
maximum and minimum values reached for a null root potassium content. Cram 1983.
compared various models involving feedback on the Im component only Table 5.. They
are of the proportional type, influx being greater when root concentration is either far
from a set point concentration error actuated feedback. or close to a minimum
concentration reciprocal feedback.. Cram 1983. concluded that error-actuated feedback
best simulated both influx and homeostasis for chloride. This choice has been criticized
by Glass and Siddiqi 1984b, 1985., and indeed a molecular mechanism for sensing a set
point concentration is hardly imaginable. However, a similar approach has been recently
proposed for nitrate influx regulation by Buysse et al. 1996..
58
Table 5
Some feedback formulas used for ion influx I . into roots. Im absolute or relative maximum influx, K
MichaelisMenten constant, x s , x cyt , x r nutrient solution, cytoplasm and root concentrations of ion X, x min
and x sp minimum and set point root concentrations of ion X
Formula
I s Im e b x r =
xs
xs q K m e b
xr
Type
Authors
feedback on Im and K m
Siddiqi and Glass 1982, 1986.
with b- 0 and b ) 0
I s Im 1y
I s Im
x min
xr
xr
x sp
=
.=
xs
xs q K m
xs
xs q K m
I s Im x sp y x cyt .=
xs
xs q K m
error actuated feedback on Im
Cram 1983.
reciprocal feedback on Im
Cram 1983.
error actuated feedback on Im
Buysse et al. 1996.
From a mechanistic viewpoint, a direct negative feedback of internal potassium and

chloride on their respective transporters is currently admitted. This is mostly supported
y
2y
by the absence of metabolism for these ions. Instead, other ions NHq
4 , NO 3 , SO4 ,
2y .
PO4 are metabolized, and feedback from their assimilation products is under examination. Indeed, when plants are treated with L-cysteine an S-containing amino acid.,
sulphate uptake is strongly depressed Clarkson et al., 1983.. Similarly, treatments with
various amino acids reduce nitrate or ammonium uptakes Lee et al., 1992; Muller
and
Touraine, 1992. while malate, a by-product of leaf nitrate and sulphate assimilation,
stimulates nitrate uptake Touraine et al., 1992, 1994.. However, reports on correlation
between root amino acid content and nitrate uptake rates remain conflicting Delhon et
al., 1995a,b; Laine et al., 1995.. As a matter of fact, the same problems arise to prove
either a direct effect of the transported ion itself or an indirect effect by its assimilation
products. Split-root experiments where part of the root system is deprived of a particular
ion, result in an increase of ion uptake by normally fed roots. For nitrate, this
enhancement is not correlated to root amino acid content Laine et al., 1995.. For both
nitrate Laine et al., 1995. and sulphate Clarkson et al., 1983., uptake rate is usually
better correlated with the non-metabolized ion content of shoots than roots. Interestingly,
the same arises for potassium Claassen and Barber, 1977., showing that such experiments are not decisive in proving a direct or indirect effect on the transporters. Even
experiments involving the use of treatments affecting nitrogen assimilation, or nitrate
reductase deficient mutants, do not prove decisive Lee et al., 1992; King et al., 1993..
Experimental uncertainties arise from the difficulty to devise experiments involving only
short-term regulations, and from the analytical significance of root ion or amino acid
content, as only the cytoplasmic content of cortical cells is expected to act on the
transporters.
2.2.2. Efflux
Few experimental data are available for efflux. A positive linear relationship between
root ion content and efflux has been demonstrated for nitrate Breteler and Nissen, 1982;
59
Mackown, 1987; Teyker et al., 1988., and a correlation between cytoplasmic ion content
and efflux have been reported for nitrate Kronzucker et al., 1995b. and ammonium
Wang et al., 1993a; Kronzucker et al., 1995c.. Efflux being considered as a passive
leak, it is usually computed as the mere product of internal concentration and a
permeability constant Cram, 1983..
2.2.3. Net uptake
Net uptake can be modelled by subtracting efflux from influx in the above models
Cram, 1983; Siddiqi and Glass, 1986.. However, an interesting endeavour to simulate
nitrate uptake under constant ion concentrations should be mentioned here. Scaife 1989.
showed realistic nitrate uptake rate patterns in the diurnal cycle using a model based on
a constant influx rate, an efflux proportional to the plant nitrate content and a nitrogen
assimilation rate proportional to photosynthesis. This model even predicted the time-lag
usually observed between maximum photosynthesis and maximum nitrate uptake rate.
Our own simulations unpublished. showed that this time-lag is not constant, but
increases from day to day when diurnal photosynthesis increases, or decreases on the
reverse situation. This behaviour is consistent with published data Clement et al., 1978..
Furthermore, diurnal variations of plant nitrate concentration are also realistic. It should
be emphasized that all these properties are typical of a capacitive model, where fluxes
are controlled by the buffer content. In fact, Scaife proposed that net nitrate uptake be
negatively correlated to plant nitrate concentration. His interpretation of parameters can
be turned round in terms of regulated influx and constant efflux; eventually both fluxes
can be regulated without changing the models behaviour. The energy cost of net uptake,
however, should be strongly affected by these different options. Most important of all,
models based on feedback from internal ion concentration Cram, 1983; Siddiqi and
Glass, 1986; Scaife, 1989; Buysse et al., 1996. are potentially able to simulate both ion
uptake and homeostasis. However, they were formulated in a context of low ion
concentration and further studies are needed in the high concentration range corresponding to horticultural practice.
2.3. Nutrient use efficiency
2.3.1. Nutrients and photosynthesis: a causal relationship?
There is an intimate relation between plant nitrogen or phosphorus status and the
carbon metabolism. Hence, N and P deficiencies in plants induce changes in carbohydrate synthesis and degradation pathways Rufty and Huber, 1983; Vessey and
Layzell, 1987; Rufty et al., 1988; Fredeen et al., 1989; Paul and Stitt, 1993.. For
instance, nitrogen-deficient tomato plants accumulate starch in their leaves which
decreases rapidly their SLA specific leaf area in m2 gy1 leaf. Suniaga Quijada, 1991;
Gary and Bertin, 1992.. Many observations made over a range of nitrogen availability in
the environment suggest the existence of a compulsory balance between nitrogen and
carbon nutritions. This explains why plants optimize their carbon gains in relation to
nitrogen available for photosynthesis Field, 1983; Hirose and Werger, 1987a,b; Lawlor,
1994.. This optimization implies a tight relation between leaf nitrogen concentration N .
and its maximum photosynthetic activity A max ., measured at saturating light intensity
60
under optimum temperature and humidity conditions at ambient CO 2 levels. Similarly,

phosphorus deficiency progressively stops aerial plant growth, decreases phosphorus
concentration in the dry biomass P . and diminishes leaf maximum photosynthetic
activity Brooks, 1986; Fredeen et al., 1989; Halsted and Lynch, 1996.. The decrease in
growth, however, results more from a lack of phosphorus for new tissue biosyntheses
leaf expansion for instance. than from a drop in photosynthesis. Thus, the observed
close A max P relation Lynch et al., 1991. comes from the indirect effect of phosphorus
on leaf expansion, which in turn affects photosynthesis. Sanders 1993. discussed this
argument and reckoned that a shortage in phosphorus affects growth via changes in the
root:shoot ratio. Reference to photosynthesis is therefore not essential in modelling plant
phosphorus nutrition. The A max N relationship has been investigated thoroughly, especially in ecological studies where nitrogen availability in the soil influences species
adaptation to their ecosystems. At the present time, only statistical models account for
the A max N relationships Table 6.. They are based on several hypotheses about the role
of nitrogen in several photosynthesis-limiting reactions Field and Mooney, 1986..
1. A max could be regulated by one or several processes functioning at rates
determined by leaf nitrogen content. For instance, the rate at which CO 2 is transported
from gaseous to liquid phases depends on the activity of carbonic anhydrase and CO 2
fixation depends on the activity of the enzyme Rubisco, on RuBP, NADPH, ATP
regenerations. All these steps require enzymes, in which the constitutive nitrogen may
be the rate limiting factor. As a consequence, the optimization of nitrogen efficiency for
photosynthetic use is made through the function of nitrogen distribution between plant
organs and between classes of nitrogen compounds.
Table 6
Mathematical functions used for modelling the effect of nitrogen on photosynthesis
Ref.
Model
Description
1.
A ma x s a= N q b
a0 = Nns
As
SLA=T
a and bs constants
2.
As photosynthetic rate,
SLA sspecific leaf area,
T s proportion of incident light in
the horizon where the leaf lies,
a 0 s constant, Nns s non-structural
nitrogen concentration
3.
4.
5.
6.
A ma x s A x =
y1.
1q e
A ma x s a= N q b= N q c
A ma x s A x = w 1y eyk N y N 0 . x
Ax = N k
A ma x s
Kpq N k
2
ya NyN 0 .
A x s maximum A max , as constant, N0 s N at zero A max

a, b and cs constants
A x s maximum A max , k s constant, N0 s N at zero A max
A x s maximum A max , k s constant, K p s N at A x r2
1. Field and Mooney 1986.; Hirose and Werger 1987b.; Sage and Pearcy 1987b.; Hirose et al. 1988.;
Evans 1989b.. 2. Charles-Edwards et al. 1987.. 3. Sinclair and Horie 1989.; Connor et al. 1993.;
Muschow and Sinclair 1994.; Bellert 1995.. 4. DeJong and Doyle 1985.. 5. Cromer et al. 1993.. 6. Lim
et al. 1990..
61
2. A max could be regulated independently from nitrogen by stomata, CO 2 diffusion

resistance, etc.. but leaf nitrogen content could be adjusted to maximum leaf photosynthetic activity. In case of nitrogen shortage, the plant would optimize nitrogen investment since any enzyme activity or nitrogen compound in excess of that strictly required
for maximum rate would be useless, only the limiting factor being worth upraising. As a
consequence, nitrogen use efficiency is highest when the distribution of nitrogen to all
non-limiting plant growth processes is regulated towards the critical N concentration.
3. A max and N could not be adjusted one to another but be both regulated by one or
several leaf parameters. In this case, A max and N would be invariant when expressed
relative to the appropriate leaf unit but would vary proportionally based on other units.
Hypotheses 1. and 2. may be put forward since they are backed by a number of
observations concerning nitrogen distribution and use in plant leaves. In a leaf, the
fraction of nitrogen used in photosynthesis is determined by the orientation of assimilates towards compounds required by photosynthesis. The latter are numerous and
almost identical in all plant cells. Hence, structural N is associated with the protection of
cell walls against biotic or non-biotic attacks, and cells contain various nitrogen solutes
such as vegetative storage proteins VSP., peptides, polyamines, alkaloids, etc.
Lambers and Poorter, 1992.. On the other hand, up to 75% of leaf nitrogen may be
associated with the functioning of the chloroplast. Nitrogen is constitutive of proteins
16 to 18% N in average. involved in CO 2 fixation and CO 2 acceptor replacement
Field and Mooney, 1986.. Ribulose-1,5-bisphosphate carboxylaseroxygenase Rubisco.,
the CO 2 fixing protein, represents more than 50% of the chloroplast soluble proteins
Evans, 1983, 1989a; Makino and Osmond, 1991.. Nitrogen is also constitutive of
pigments associated with the light-harvesting machinery 50 mol N moly1 chlorophyll.,
proteins of the electron transport chain and proteins of the CalvinBenson cycle Abadia
et al., 1987; Nishio et al., 1985; Wong et al., 1985.. Moreover, nitrogen is found in
nucleic acids, the peroxisome and in mitochondria enzymes responsible for the renewal
of products during photorespiration. At last, according to environmental conditions
incoming radiation., nitrogen may be allocated in priority to compounds involved in the
light phases of photosynthesis pigments, photosystems, etc.. or those concerned with
the dark reactions Rubisco, CalvinBenson cycle proteins, etc... Acclimatization to
shade induces a lower nitrogen investment in light harvest Evans, 1989a..
2.3.2. Seeral models
In a comparison of a plentiful number of plant species characteristic of natural
ecosystems, Field and Mooney 1986. observed a tight linear relationship between A max
and N when both parameters were expressed per unit of leaf dry matter. This could
indicate a general law. However, expressing data per unit leaf area, which is more
satisfactory from a physiological viewpoint, may result in differences which are
attributed to SLA variations between plants of different leaf N status. Several models
have been proposed so far to account for the A max N relation Table 6.. For several
species, this relation is not linear but hyperbolic. Hence, for these species, from low leaf
N onwards, A max increases rapidly with increasing N but reaches a plateau where N
accumulation is no longer beneficial to photosynthesis. According to Evans 1989a., the
curvature of the relationship does not reflect an inactivation in Rubisco at high leaf N
62
but could result either from 1. an underestimation of A max or 2. a decrease in CO 2

partial pressure in the leaf between the intercellular space and the site of carboxylation
because of an increase in the resistance of cell walls to CO 2 transport. According to
Sage and Pearcy 1987b., the loss of linearity in the A max N relation proceeds from the
appearance of nitrogen storage compounds in the leaves nitrate, asparagine, etc...
The ratio A maxrN is called the photosynthetic nitrogen use efficiency PNUE.. It
removes the effects of fluctuating SLA and allows the comparison between species to be
carried out. Several studies have shown that the efficiency of C 4 species is higher than
that of C 3 species, which has been interpreted as the result of a better acclimatization to
environments low in nitrogen Brown, 1978; Sage and Pearcy, 1987a,b.. However, the
reduced rates of photorespiration in C 4 species gives also these plants higher A max
values than C 3 plants. In this case, higher PNUE may also proceed from a better use of
carbon. The difficulty of interpreting PNUE data comes from the fact that in a ratio,
similar data may result from equal changes either in the numerator or the denominator.
Within a similar photosynthetic type, however, changes in PNUE have been reported
Field and Mooney, 1986; Lambers and Poorter, 1992.. These could reflect interspecific
differences in Rubisco activity or nitrogen allocation towards the functioning of this
enzyme Evans, 1989a. as well as intra-specific differences in nitrogen allocation
towards compounds not involved in photosynthesis or involved but not limiting photosynthesis.
Most horticultural crops being fast growing species, it is reasonable to assume that
their leaf nitrogen is invested in priority towards photosynthetic compounds. Therefore,
leaf nitrogen analysis is a potential tool for assessing the limiting or non-limiting nature
of nitrogen in crop photosynthesis using the A max N relationship typical of the species.
Moreover the calculation of the PNUE index indicates the closeness of nitrogen supply
to the demand of the crop. Any supra-optimal nitrogen availability results in nitrogen
accumulation in plant tissues and thereby decreases PNUE compared with pre-defined
optimal value. This index could therefore be used as an indicator for nitrogen fertilization decision making. This index, however, should be considered with care since a
PNUE increase is not necessarily beneficial to plants. For instance a PNUE increase has
been observed in nitrogen-deprived rose plants Bellert, 1995. together with a decrease
in A max . In this case, the decrease in leaf N concentration more than offset the decrease
in A max , thus yielding higher PNUE. This was interpreted as the result of a greater
remobilization of non-photosynthetic nitrogen under nitrogen shortage, hence, rendering
the remaining nitrogen more efficient for photosynthesis.
2.3.3. Nutrients and water fluxes
Stomata are a compulsory passageway for CO 2 and H 2 O gas exchanges between the
plant and the atmosphere. Therefore, in order to fix carbon, the plant looses water to the
atmosphere, the ratio being variable depending on species and growing conditions. This
ratio is called the water use efficiency WUE., i.e., the quantity of water transpired per
unit carbon fixed in the dry matter. Plants under conditions of low water availability
andror great water demand have low stomatal conductance and low leaf CO 2 partial
pressure. Therefore, these plants have low WUE because the decrease in their rate of
transpiration is larger than the decrease in CO 2 fixation. Under such circumstances, the
63
low A max values associated with normal leaf nitrogen concentrations, also give these
plants low PNUE indices. The measurement of the isotopic ratio 13 Cr 12 C is an
assessment of plant WUE. It has been introduced as a tool for geneticists in breeding
programs to select plants with low water use efficiency Evans and Farquhar, 1991..
Similarly, Masle et al. 1992. suggested that plant breeders use plant mineral concentration as an alternative measurement, simpler and economically more viable than isotopic
ratio determinations. Hence, these authors observed positive correlation between WUE
and mineral concentration in the dry matter of several C 3 and C 4 species.
2.3.3.1. Is there a causal relationship between PNUE or mineral concentrations and
WUE? Is mineral uptake, in particular nitrogen, controlled by plant water fluxes? In a
study made on several herbaceous species, Lambers and Poorter 1992. were able to
observe the doubling of PNUE index in plants of constant WUE. Similarly, Field and
Mooney 1986. measured the same isotopic ratio 13 Cr 12 C in C 3 species of markedly
different PNUE index. Therefore, in light of the present evidences, we may seriously
doubt a causal and general relation between PNUE and WUE. Moreover, Barthes et al.
1995. observed for two wheat species widely different rates of mineral accumulation in
the whole plant, and concluded that the measurement of mineral concentration in the
tissues could not be proposed as an alternative measurement to the d 13 C isotopic ratio
normalized against an absolute reference. and thereby to WUE. At last, Tanner and
Beevers 1990. found that two lots of maize plants grown in controlled cabinets under
two contrasting regimes of relative humidity RH s 60 or ) 95%. had on the one hand
a WUE differing by a factor 3.3 and on the other hand, a same dry matter yield
production and a similar plant mineral content at the end of the crop cycle.
The questions addressed above are fundamental in horticulture. For instance, in the
practice of soilless culture, the frequency of delivery of nutrient solution doses to the
crop is determined almost solely by plant water demand estimated from incoming solar
radiation. Underlying in this practice is the hypothesis that the requirements for water
and for minerals are always intimately correlated. The experiments made over long
periods of time weeks, months. generally support such an hypothesis Brun and Blanc,
1987; Schacht and Schenk, 1990; Bar-tal et al., 1994. and have led agronomists to
empirical determinations of recipes for ideal ion mixtures adapted to plant growth
stages. On the contrary, experiments made over short periods of time hour, dayrnight
cycle. demonstrate clearly that the ratio of water to nutrients taken up by the plants vary
widely with time of the day Tribo-Blondel,
1979; Le Bot, 1991; Ferrario et al., 1992;
Le Bot and Kirkby, 1992; Andriolo, 1995; Brun et al., 1997.. Moreover, during summer,
and in particular under Mediterranean conditions, growers observe frequently a sharp
and rapid increase in the nutrient solution salinity, potentially at risks for both the plants
and the environment. This happens because during such periods of time, plant water
demand increases more than mineral requirement.
All these evidences support the idea that the transpiration flux is not essential to ion
uptake and transport in plants, and therefore in plant nutrient uptake modelling it is
necessary to dissociate mineral fluxes from water fluxes. A model of ion uptake simply
based on plant transpiration flux has no scientific grounds, neither does the calculation
or use of uptake concentrations i.e., the ratio of ions to water taken up over time.. In
64
spite of these statements, the actual practice of fertilization of soilless cultures grown
under greenhouses with drainage-to-waste bases the supply of nutrients on plant water
demand models de Villele,
` 1972.. This modelling of nutrient supplies is successfully
operative in most commercial greenhouses yet it has extremely poor predictive properties as proven by 1. the occurrence of the drifts in nutrient solution salinity requiring
heavy washing of the rockwool slabs with diluted nutrient solution and 2. the poor
coefficients of fertilizer use i.e. the ratio of fertilizer taken up by the plants to that
applied in the slabs., especially for nitrate van Noordwijk, 1990., which are of serious
environmental concern, especially in intensive areas of greenhouse production. These
conclusions, however, should not hide the fact that in soil, the transpiration flux is the
driving force for the transport of most mineral ions from the soil layers to the roots, and
therefore, it is essential for modelling nutrient availability at the soilrroot interface.
3. Ultimate functions
3.1. Nutrient uptake and functional equilibrium
Plant nutrient uptake rate is computed as the product of net uptake rate per root unit
Section 2.1.. by the size of the root system. The latter, usually characterized by the
RSR root:shoot ratio. or RWR root:whole plant weight ratio., varies greatly between
species, edaphic conditions and with plant age. For instance, Laine et al. 1993. found a
negative relationship between nitrate uptake capacity per root unit and RSR from 0.1 to
1. in ten catch crop species grown under non-limiting constant nutrition. However, when
we computed their data to express them per total plant fresh weight, uptake capacity was
roughly the same for all these species, showing that a similar absorption rate can be
achieved by various plant strategies. Similarly, it is commonly observed that most plants
increase the size of their root system when water or nutrients particularly nitrate and
phosphate. are limiting, or decrease it under low light conditions. However, under
non-uniform nutrient supplies, root growth is usually stimulated in the well-fed zone,
while it can be depleted in the restricted zone for review, see Habib et al., 1991;
Robinson, 1994.. From the nutritional viewpoint, the importance of these strategies
depends upon if the root medium is homogeneous e.g. hydroponics. or heterogeneous
e.g. natural soil.. From a carbon utilization viewpoint, high RSR differences are
necessarily important since roots represent from 1 see Table 1 in the work of Marcelis
and De Koning, 1995. to 50% Laine et al., 1993. of plant dry weight.
Mechanisms involved in RSR elaboration are unclear for review of opinions, see the
special issue of Plant and Soil, 185, 1996.. They include specific root growth regulation
by plant hormones cytokinins and abscisic acid. or sucrose, and non-specific determination by the so-called functional equilibrium Brouwer, 1962; see also Marcelis et al., this
issue.. In the latter, RSR may be seen as an emergent property, resulting from the
balance between root and shoot growth necessary to acquire the limiting resources,
nutrients and carbon, respectively. To achieve such models, it is necessary to formalize
dry mass production under nutrient limitation, nutrient uptake under carbon limitation,
and rules of carbon and nutrient exchanges between roots and shoots.
65
It is beyond the scope of this review to develop all these aspects but it should be
stressed that existing models lay on unregulated root uptake activity. The latter is either
expressed as only proportional to the size of the root system Cheeseman, 1993;
Reynolds and Chen, 1996., or following the MichaelisMenten kinetics of Epstein and
Hagen Lim et al., 1990.. Although such models do predict the right tendency of RSR
variations, such oversimplified assumptions should result in exaggerated changes, as the
only way to increase nutrient uptake rate is to increase the size of the root system. A
more realistic approach requires the use of nutrient uptake feedback regulation Section
2.2.., which implies, therefore, the modelling of nutrient accumulation and assimilation
rates Buysse et al., 1996.. This should result in more realistic effects of nutrient
limitation, i.e. increase of both RSR and SAR specific absorption rate.. Furthermore,
more research is required on transport of resources between compartments. It is viewed
as a purely diffusive process where flux is along a concentration gradient affected by a
resistance parameter Thornley, 1972, 1995., an active process following a Michaelis
Menten relationship whose substrate is the concentration in the source compartment
Cheeseman, 1993., or the much-controversial xylemic water transport process where
flux is determined by transpiration for review, see Tanner and Beevers, 1990..
Choosing between these possibilities is uneasy, as nitrate concentration in the shoots of
several species has been reported to be higher than, equal to or lower than that of roots
Laine et al., 1993.. This might explain why less mechanistic approaches may be
preferred. These include a simple partition coefficient where a constant proportion of the
mineral is allocated to roots and shoots Siddiqi and Glass, 1986., or sophisticated
models of sourcesink relationships, where flow between compartments is governed by
the size of the source and growth rate of the sink Ran et al., 1994..
3.2. Growth control by nutrients
The general idea that nutrient availability in the root medium determines plant growth
arises from the general concepts of the limiting factor von Liebig, 1841.. An original
use of this concept has been developed since the seventies by Ingestad and Cottorkers
for review, see Ingestad and Agren,

1992.: their technique consists in supplying
nitrogen at constant relative addition rates RAR. to hydro- or aeroponically grown
plants. As long as nitrogen remains limiting, they show that the plant relative growth
rate RGR. equals RAR, and that whole-plant nitrogen concentration is nearly constant.
On this ground, Ingestad introduced the term of steady-state nutrition. This technique
has been used on a large number of plants and was shown to hold also for phosphorus
Ericsson and Ingestad, 1988., and is probably generalizable to other macronutrients.
On the one hand, there is no doubt that this technique is a valuable tool to monitor
growth under controlled conditions. On the other hand, theoretical considerations have
been derived to interpret the relationship between plant nutrient content and RGR
Agren,
1985, 1988.. Whether these have sound physiological background or not is
under debate for opinions, see Macduff et al., 1993; Burns, 1994; Wikstrom
and Agren,
.
1995; Hellgren and Ingestad, 1996; Burns, 1997 and their use for diagnostic procedure
for crop nutrient management Burns, 1997. or for modelling nutrient uptake by
horticultural crops Willits et al., 1992. are far from being straightforward. Hence, the
66
parameters of the relationship linking plant nutrient content to RGR are not unique, but
vary according to plant species Agren,

1988., plant age and environmental conditions
Willits et al., 1992..
3.3. Growth demand of nutrients
3.3.1. Statistic approach
Minerals are taken up by the roots and eventually assimilated. in order to fulfil plant
growth requirements. For nitrogen, phosphorus and potassium it has been demonstrated
at all times of the vegetative crop cycle, that a critical concentration is required in plant
tissues to sustain 90% of the maximum growth rate potentially obtained by the amount
of radiation intercepted by the crop Ulrich, 1952; Burns, 1990.. Below the critical
concentration, growth is impaired. On the contrary, if nutrient availability is excessive,
nutrients accumulate in the plant without concomitant increase in dry biomass. The
implicit relationship between nutrient uptake and dry matter accumulation s growth.
during the vegetative development of a crop is particularly well expressed for nitrogen
in the law of progressive decline of %N g total N 100 gy1 dry matter. during crop
growth Lemaire and Salette, 1984; Justes et al., 1994.:
%N s a = DMyb
where: DM tonnes hay1 . is the total dry aerial biomass, %N is the critical nitrogen
concentration, coefficient a represents the nitrogen concentration in the dry biomass at
the end of the exponential growth period, and b is a statistical parameter governing the
slope of the relation.
This relation implies an allometry between nitrogen uptake by the crop N, kg hay1 .
and the dry matter biomass accumulation:
N s 10 = a . = DM 1y b
where: 1 y b . is the ratio between the relative rates of N uptake and dry matter
accumulation allometric parameter. and 10 = a . is the amount of nitrogen kg. taken
up by 1 ha of the crop at the end of the exponential growth i.e. about 1 tonne DM hay1
for most crops..
The practical interest of such a relationship comes from the prediction of the
minimum nitrogen fertilization required by the crop to produce a targeted dry matter
yield. Greenwood et al. 1990. have established that critical N concentration of a great
number of plant species fit one out of two possible relationships providing that they
belong either to the C 3 or C 4 type of photosynthesis. Many authors agree on the idea
that the parameter b is identical for C 3 and C 4 species while a is specific for the type
of photosynthesis. Various estimates of the parameters have already been published in
the literature but the later review on the subject Lemaire and Gastal, 1997. proposes the
following average relations:
for C 3 species: %N s 4.8 = DMy0 .34
for C 4 species: %N s 3.6 = DMy0.34
67
These findings may be interpreted as an indication that under non-limiting nitrogen

supplies, C 4 species are 25% more efficient than C 3 species in accumulating the same
amount of dry matter with a same quantity of nitrogen taken up. This better nitrogen use
efficiency determined at the large time scale supports the findings of higher PNUE index
of C 4 species measured over short time scales, as already discussed in Section 2.3.
However, the argumentation developed earlier of a higher carbon use in C 4 species
because of low photorespiration also leads to the same conclusions. The finding of a
unique parameter a between C 3 and C 4 species grown on 1 ha of land suggests that
nitrogen use is identical in all plants, irrespective of their carbon metabolism, and is
essentially determined by light interception.
The general relationship of progressive decline in %N in the dry biomass of plants
has been verified for a large set of crop species which confers this relation the status of
law, at least for non-ligneous plants free of storage organs. A more detailed analysis of
the literature can be found in the work of Justes et al. 1994. and Lemaire and Gastal
1997.. For horticultural crops, to our knowledge, only tomato has been evaluated. For
this species, the progressive decline in %N has been shown to hold both for vegetative
and fruiting plants Andriolo, 1995; Le Bot et al., 1997a; Bellert et al., 1997., although
for the time being, a precise relationship using critical nitrogen values has not yet been
established. However, under non-limiting nitrogen supply, Andriolo 1995. determined
the following relation: %N s 5.77 = DMy0 .33. For this particular species, it is interesting to note that the concept of progressive decline in %N values, which was first
developed over the vegetative growth of field crops having a closed canopy structure,
also holds for the entire cycle of a row crop with indeterminate growth.
3.3.2. Mechanistic approach
Two mechanistic models explain the progressive decline of %N in the dry biomass in
terms of plant compartmentalization. For Caloin and Yu 1984. plant nitrogen content
varies during growth according to the proportion of two conceptual compartments in the
plant. The first compartment is physiologically active for growth; its dry mass M1 . is
related to the rate of total dry mass increase E MrE t . by the following relation:
EM
s RGR max = M1
Et
RGR max being measured during the exponential growth phase. Along growth, the
proportion of M1 in plant is:
M1
1
1
EM
RGR
p1 s
s
= =
s
M
RGR max
M
Et
RGR max
The second compartment has a mass M2 s M y M1 .. It is involved in the other
metabolic activities of the plant, including structures and storage. Caloin and Yu 1984.
propose to give both compartments M1 and M2 . different nitrogen concentrations
although constant over time, i.e. n1 and n 2 g N 100 gy1 DM.. At any time t . of the
crop growth, total plant nitrogen content N . may be calculated from the size of the two
compartments:
N t . s n1 = M1 t . q n 2 = M 2 t .
68
therefore, total nitrogen concentration n. is:

N t.
n t . s
M t.
sn1 = p 1 q n 2 = 1 y p 1 . sn1 =
RGR
RGR max
q n2 = 1 y
RGR
RGR max
that is,
n t . s
n1 y n 2
RGR max
= RGR q n 2 s a = RGR q b
In contrast to other approaches see Section 3.2.., in this model the relative growth
rate is not a forcing variable for nitrogen uptake but its measurement gives a good
determination of the sizes of the two compartments. From practical viewpoints, the
linear relationship between RGR and plant nitrogen concentration has been verified in
the case of several cultivated species. However, a generalization of the model parameters has not been established yet, which appears as a limitation compared with the
statistical approach developed above Section 3.3.1...
A second model Hardwick, 1987. has been developed from studies on woody plants.
It assumes that plants are composed of an external skin of energetically active tissues
covering a three dimensional inner core which does not engage in energy exchange. In
a closed canopy structure, the mass of skin K . is proportional to the area of light
interception; it is therefore proportional to the square of plants length l ..
Moreover, the mass of the whole plant W . is proportional to the volume of the plant,
i.e. the cube of plants length:
Ksc=l2 Wsd=l3
where c and d are constants of proportionality. Replacing l in the first equation results
in the following expression:
2
KAW 3
Some evidence supports the idea that the amount of skin is proportional to plant
nitrogen content Sylvester-Bradley et al., 1990; Le Bot et al., 1997b.. In this case, for a
young plant in which the mass of core is negligible, increase in the amount of skin is
mirrored by a similar increase in plant nitrogen content N .:
EN
EW
s 1 that is, N A W
For an adult plant, however, the core becomes predominant. Therefore, the total plant
mass is a good estimate of the mass of core, which implies that:
EN
EW
2
s
3
that is, N A W 0.66
According to Hardwick 1987., for a given species, there is a curvilinear relationship

between the nitrogen content of a plant and its total biomass, the slope of the curve
69
varying between 1 and 0.66. Hardwick proposes the following mathematical formula to
fit the relationship:
y s p q q = x . q r = eyx .
where: y s log nitrogen mass per plant., x s log total plant biomass., r, p and q are
constants determined by the initial plant biomass and allometric parameters relating
length to surface and volume plant dimensions. Rewriting this equation leads to:
r
Nsk=e W =W q
Therefore, when W `., as is the case in an adult plant, this expression yields the
same formula expressed by Lemaire and Salette 1984. and already developed above:
Nsk=W q
In conclusion, both models of Caloin and Yu 1984. and Hardwick 1987. explicate
dynamically the reasons for the progressive decline of %N in the dry matter from the
existence of two compartments having different physiological functions and biochemical
compositions. In both models, however, the two compartments are virtual and remain to
be studied further. Hardwick associates the skin with the tissues responsible for the
process of life, which include the foliage, responsible for energy income, but also the
fractions of roots, responsible for ion uptake, while the core is associated with tissues
comprising cellulose, starch and lignin which do not require maintenance costs. In the
model of Caloin and Yu, compartment M1 presumably comprises foliage and root
fractions while compartment M2 should be composed of the structures holding the
foliage in position and storage tissues. It is only if plant compartmentalization is
associated with a more precise anatomical description of the appropriate tissues that a
validation will be possible. More work is therefore required on that subject, although a
first attempt to fit the model of Caloin and Yu to ageing tomato plants, led Bellert et al.
1997. to separate the foliage rich in nitrogen 4 g N 100 gy1 DM. from the stems,
petioles and fruits low in nitrogen 1.8 g N 100 gy1 DM..
4. Operational approach of nutrition

4.1. Diagnostic of nutritional status
The appraisal of substrate fertility and the assessment of plant mineral requirements
are fundamental for crop fertilization management. In practice, the cultural system
should be optimized in accordance with expectations on yield, crop quality of harvested
or transformed organs. or environmental concerns residues in the soil for instance.. The
estimation of nutrient availability for plant growth is generally achieved through soil
substrate. testing, which is more or less convenient depending on the agrosystem, or
through plant or sap analysis. For soilless cultures, technology is providing on-line
sensors pH, electrical conductivity EC. to monitor ion concentrations, which make
possible the short-term management of nutrition see Section 4.2... In orchards, the
measurement of minute changes in stem diameter can be used to manage irrigation
70
Huguet, 1985.. Whole-plant testing is also widely used because it gives a direct
measurement of the actual quantities of nutrients taken up by the crop. When testing is
not possible on the entire plant, analysis of individual organs leaf, petiole, etc.. is often
taken as a substitute. In such cases, the mineral concentration measured in plant tissue is
compared to that of reference material obtained from plants grown under non-limiting
nutrient supply. The increasingly widespread use of leaf analysis since the fifties has
resulted in exhaustive compilations of normal, deficient or toxic nutrient concentrations in plants Chapman, 1966; Martin-Prevel
et al., 1984.. Following this approach, it
seems that each tested plant has its own nutrient deficiency concentrations which may
appear irrational considering the similitude in metabolism between different species.
However, it is evident from the modelling approaches developed in Sections 3.2. and
3.3. that a sensible interpretation of analytical data for diagnostic purposes requires
knowledge of the plants critical nutrient concentrations over the whole growing cycle.
For example, the diagnostic of nitrogen nutrition is an immediate and practical output of
the critical N concentration model see Section 3.3... Hence, during plant growth,
nitrogen concentration in the plant tissues may be compared to the critical nitrogen
concentration thus allowing calculation of a nitrogen nutrition index NNI.:
NNI s
%N
%Ncritical
As long as NNI is greater than 1, crop growth is not limited by nitrogen availability
in the root environment. When NNI is lower than 1, the rate at which the crop grows is
limited by nitrogen uptake. Hence, increasing nitrogen availability in the root environment may increase the crop growth rate. In this case, NNI may be used as a
decision-making indicator to provide the crop with an extra dressing of nitrogen
fertilizer. This approach also provides an ubiquitous rationale for diagnostic that may
probably be extended to minerals other than nitrogen. Hence, phosphorus and sulphur,
which are also taken up as anions H 2 PO42y and SO42y . and undergo a step of reduction
in plants, should obey similar laws of progressive decline in critical concentrations in
the dry biomass. Moreover, due to similarities in their metabolisms, we may speculate
that the parameters of the progressive decline of %P and %S should be similar to that of
nitrogen. For cations, it is probable that potassium, which is the largest counterbalancing
ion for nitrate uptake, also follows similar pattern. Calcium and magnesium, however,
are likely to require different modelling approach due to the importance of plant cation
exchange capacity CEC. and water fluxes in uptake and transport of these two divalent
cations.
4.2. Managing the cultural system: the greenhouse as an example
The actual development of protected cultural systems is characterized by an increase
in soilless techniques and the automatic monitoring of climate and fertilization. Such
systems are costly in respect to hand-power and energy inputs. Optimizing these
high-tech systems requires the use of models describing fluxes of mass and energy in the
plant in harmony with those described for the environment Baille, 1997; Gary and
Baille, 1997.. In terms of fertilization, the widespread use of on-line programmable
71
fertilizer injectors gives growers an opportunity to apply the current scientific knowledge to greenhouse crop fertigation, for instance the uncoupling between water and
nutrient supplies. The analysis of current practices reveals a dual approach for controlling plant nutrition, i.e. inductive or deductive regulations.
1. In open run-through. or closed types of soilless cultures, the actual practice of
fertigation consists in providing the crop with doses of nutrient solution at pre-set pH
and electrical conductivity values EC t .. As long as water and nutrients are taken up at
dr .
dr .
the same rates, EC in the drainage EC meas
remains close to a reference value EC ref
.
In case of drifts, the nutrient solution concentration can be altered based on the
difference between the reference and measured EC in the drainage. Therefore at any
time t ., EC may be determined from the previous EC of the nutrient solution supplied
at t y 1.:
EC t s EC ty1 = 1 q
dr
dr
EC ref
y EC meas
dr
EC ref
However, EC measurement is partially relevant to the system since it provides only

limited control of fertigation. Indeed, it is an indiscriminate indicator of the overall
concentration of fertilizers in solution while the appropriate blending of several mixtures
of fertilizers requires a precise adjustment of individual ion concentration. Therefore, the
inductive a posteriori. regulation exhibits two main limitations: 1. the absence of
specific sensors reliable in greenhouse conditions, and 2. the time-lag of the horticultural systems 25 days for fertigation in rockwool slabs. is incompatible with the
hourly control of nutrient feed targeted by the regulator. In our view, the success of this
type of regulation is linked to a straight forward technological breakthrough in the
construction of reliable ion specific sensors, in particular for nitrate measurements in
drainage. Also required are changes in the root system environment. It will be necessary
to find a compromise between the current inertia of the system which is stable and
secure, and the regulation time-lag requirements on which depend the optimization of
the system.
2. The deductive a priori. regulation is potentially ideal to optimize the control of
greenhouse crop mineral nutrition. It is based on the knowledge of plant responses to
varying its environment. Plant water supply based on calculation of potential evapotranspiration ETp . belongs to this type of approach. It allows the precise short-term
prediction of plant water demand based on the measurement of current environmental
parameters. For tomato plants growing under the greenhouse, de Villele
` 1972. proposed
to estimate ETp from the measurement of global radiation and parameters typical of the
greenhouse and the crop growth stage. Using this approach in plant fertilization should
offer two main advantages: 1. the quality of the regulation is independent of the inertia
of the system and no compromise is required between security and efficiency; 2. the
needed climatic sensors already exist in most greenhouses since they provide inputs for
climate regulation. It is therefore possible to make use of the actual systems without any
more technological inputs. The success of this approach, however, is linked to the
prerequisite knowledge of the relevant parameters; thus, modelling plant response to
fluctuating environment is essential. For the time being, no knowledge-based plant
72
Mathematical formulation
Authors
ETp s 0.67= R g y0.2

SLI C ySLI A
DLI C yDLI A
DRH C yDRH A
DTC yDTA
CD
NF s NI = x 1
q x2
q x3
q x4
q...q
SLI A
DLI A
DRH A
DTA
100
R g dy 1
.q1.435=10y2 =Tsol
Nu s 0.796=10y3 = R g =
Rg d
de Villele
` 1972.
Papadopoulos and Liburdi 1989.
Brun and Chazelle 1996.
Abbreviations: ETp , potential evapotranspiration; R g , total incident radiation; NF and NI , final and initial nitrogen concentration in solution; SLI C and SLI A , current
and average seasonal light integrals; DLI C and DLI A , current and average daily light integrals; DRH C and DRH A , current and average daily relative humidity; DTC
and DTA , current and average daily air temperature; CD, overall growers rating of crop demand for Nitrogen; x i , scalars; Nu , NO 3 uptake rate mg N planty1 hy1 .;
Tsol , temperature of nutrient solution.
Table 7
Examples of deductive models used to control water or nitrogen supply to greenhouse crops
73
model is operational to optimize the practice of mineral nutrition. Nevertheless, research

along these lines is active and most relevant parameters controlling ion uptake are
known. Current deductive regulation of ion concentration in solution is simply based on
statistical models Table 7.. For instance, Papadopoulos and Liburdi 1989. use numerous parameters influential for nutrient requirement i.e. light, RH, fruit load, crop age,
etc.. to adjust the base values of nutrient feed for tomatoes. Hence, for nitrogen as an
example, the final concentration w NF x in solution equals the initial value before
adjustment w NI x corrected by the difference between current index C. and average
index A. values of seasonal light integral wSLIx, daily light integral wDLIx, daily relative
humidity wDRHx and daily air temperature wDTx. The influence of each component is set
by scalars w x 1 x to w x 4 x %. and an overall growers rating of crop demand for nitrogen
wCDx. Another illustration is given by the work of Brun and Chazelle 1996. on roses.
They described the kinetic of nitrate uptake w Nu x mg N planty1 hy1 . with a multiple
regression using agroclimatic factors, i.e. global radiation w R g , W my2 x, global radiation
of the previous day w R g dy 1 x, the expected global radiation of the day w R g d x and the
temperature of the nutrient solution w Tsol x. This relation was strong enough to fit
successfully r 2 s 0.71. hourly uptake rate data obtained under greenhouse conditions
over a period of 5 consecutive days.
To summarize, the inductive regulation is set on a purely technological breakthrough
and is rapidly operational while the deductive regulation depends on knowledge and
requires models. The use of the former in mineral nutrition implicates that the agrosystem undergoes normal climatic fluctuations and that action takes place only after an
alteration of the system has occurred. In other words, the regulator is set to repair
accidents. The application of the latter regulation, should prevent the occurrence of
alteration in the agrosystem. Moreover, the use of climatic parameters to control plant
nutrition should lead to a more integrated greenhouse management, in harmony with the
regulation of water and carbon fluxes at the crop level. Since all physiological plant
functions obey the same stimuli, a global model appears essential to understand truly the
interactions and optimize the functioning of the greenhouse.
5. Conclusions
For the purpose of this review, we segregated nutrient uptake into proximate and
ultimate functions. This was a mean to classify the concepts according to their
spatio-temporal level of approach, as needed for modelling. Another prerequisite is
knowledge of the agricultural system. For instance, in the present understanding of plant
physiology, the role of water fluxes through plants is negligible for uptake of most
nutrients. However, depending on the agrosystem, the flux of nutrients from the bulk
substrate to root surface may be limited by water fluxes, i.e. plant transpiration.
Therefore, in field conditions, diffusion barriers may overrule uptake kinetics, while in
hydroponics, the solution stirring or circulation ensures nutrient availability at the root
surface, and transpiration is clearly uncoupled from nutrient uptake. What is more, in
intensive horticultural agrosystems, the technology allows, up to a certain extent, the
monitoring of plant nutrition without reference to physiological knowledge. In this case,
74
models are concerned with optimizing the physical system itself i.e. faster response
time, sensors, etc.. rather than understanding plant functioning. This latter approach
should not be neglected as it is probably the nearest to implementation.
Among proximate functions, most studies have been based on the concept of ion
transporters and their response to low ion concentrations, which seriously limits their use
in horticultural crop models dealing with a rich ionic environment. These studies
generally do not take plant demand into account, and therefore, are unable to provide the
necessary feedback regulation of uptake. As a consequence, they cannot make the link
with environmental conditions irradiance, CO 2 enrichment, etc.., nor predict nutrient
accumulation, which is a weakness for diagnostic purposes and quality prediction.
Furthermore, realistic estimations of respiratory costs of ion uptake, required by carbon
models, will not be made without a better understanding of uptake mechanisms and
regulation. Similarly, we may highlight the lack of models of nutrient transport and
partitioning in tissues, which are required to understand the efficiency of their use for
growth and RSR equilibrium.
Though plentiful, the literature on plant nutrition rarely serves modellers in the
development of general concepts applicable to agronomic conditions. For instance,
under different experimental conditions, i.e., steady-state vs. constant nutrition, the same
formula relates nitrogen concentration in whole plant tissue to relative growth rate:
n t . s a = RGR q b
The parameters of the relation, however, have different values and are interpreted in a
distinct way according to the context: in terms of nutrient productivity Agren,

1985,
1988. or plant compartmentalisation Caloin and Yu, 1984.. The former concept
explains growth by the plant nutrient content, while in the latter, the nutrient content is a
result of growth. This underlines the weakness of these theories in formulating functionally the interaction between growth and nutrients. Nevertheless, the steady-state approach shows that at large-time scales, the amount of nutrients added to the medium is
more determinant than their concentration, for growth. It thus turns out that a definition
of plant demand is the relevant ultimate function for modellers. Mankin and Fynn 1996.
proposed a general formulation of the demand approach:
Un s Dn " X n
where Un and Dn are the actual uptake and plant demand, respectively, while X n is
luxury consumption when positive, and storage mobilisation when negative. Plant
demand, computed from growth rate and a critical nutrient concentration, may be seen
as the basis for fertilisation policy. Interestingly, critical concentration has been shown
to depend strongly on canopy structure in relation to light interception, and on
photosynthetic metabolism, more than on other species-dependent characteristics
Hardwick, 1987; Lemaire and Gastal, 1997.. It should thus be emphasized that plant
nutrition borrows the concepts used in carbon models. However, in the present nutrition
studies, growth is seen as a mere dry weight increase. We may speculate that further
improvements could arise from the use of recent growth models, which introduced the
concepts of structural and non-structural dry matter.
75
References
Abadia, J., Rao, I.M., Terry, N., 1987. Changes in leaf phosphate status have only small effects on the
photochemical apparatus of sugar beet leaves. Plant Sci. 50, 4955.
Agren,
G.I., 1985. Theory for growth of plants derived from the nitrogen productivity concept. Physiol. Plant
64, 1728.
Agren,
G.I., 1988. Ideal nutrient productivities and nutrient proportions in plant growth. Plant Cell Environ.
11, 613620.
Alloush, G.A., Sanders, F., 1990. Responses of chickpea to iron stress measured using a computer-controlled
continuous-flow hydroponic system. In: van Beusichem, M.L. Ed.., Plant NutritionPhysiology and
Applications. Kluwer Academic Publishers, Dordrecht, pp. 197206.
Andre,
M., Daguenet, A., Massimino, D., Vivoli, J.P., Richaud, C., 1979. Le laboratoire C 2 3A. Un outil au
service de la physiologie de la plante entiere.de mesure associes.
` Les chambres de culture et les systemes
`
Ann. Agron. 30, 139151.

Andriolo, J.L., 1995. Analyse des flux de NO 3-, H 2 O et CO 2 au cours de la culture et du nycthemere
` chez la
tomate Lycopersicon esculentum Mill.. adulte en hors-sol. These
` de Doctorat, Universite de Montpellier
II, 101 pp.
Andriolo, J.L., Le Bot, J., Gary, C., Sappe, G., Orlando, P., Brunel, B., Sarrouy, C., 1996. An experimental
set-up to study carbon, water, and nitrate uptake rates by hydroponically grown plants. J. Plant Nutr. 19,
14411462.
Aslam, M., Travis, R.L., Rains, D.W., 1996a. Evidence for substrate induction of a nitrate efflux system in
barley roots. Plant Physiol. 112, 11671175.
Aslam, M., Travis, R.L., Rains, D.W., Huffaker, R.C., 1996b. Effect of root pertubation and excision on
nitrate influx and efflux in barley seedlings. Physiol. Plant 97, 425432.
Baille, A., 1997. The energy cycle. In: Enoch, H.Z., Stanhill, G. Eds.., Ecosystems of the World. The
Greenhouse Ecosystem. Elsevier, Amsterdam, in press.
Bar-tal, A., Feigin, A., Rylski, I., Pressman, E., 1994. Effects of root pruning and NNO 3 solution
concentration on nutrient uptake and transpiration of tomato plants. Sci. Hortic. 58, 7790.
Barthes, L., Deleens,
E., Bousser, A., Hannachi, L., Gate, P., Prioul, J.R., 1995. Variations of wheat leaf C
and N isotope compositions after crop fertilization. C.R. Acad. Sci., Science de la vierBiologie et
Pathologie Vegetale,
Paris 318, 253262.

Bellert, C., 1995. Gestion du carbone et de lazote par le rosier miniplant Rosa hybrida cv. Sonia.. Effets
dune privation en azote a` la pre-floraison.
These
` de Doctorat, Universite de Montpellier II, 115 pp.

Bellert, C., Le Bot, J., Dorais, M., Lopez, J., Gosselin, A., 1997. Nitrogen accumulation and growth of fruiting
tomato plants in hydroponics. Acta Hortic., in press.
Benlloch, M., Moreno, I., Rodriguez-Navarro, A., 1989. Two modes of rubidium uptake in sunflower plants.
Plant Physiol. 90, 939942.
Ben Zioni, A., Vaadia, Y., Lips, S.H., 1971. Nitrate uptake by roots as regulated by nitrate reduction products
of the shoot. Physiol. Plant 24, 288290.
Berlier, Y., Guiraud, G., Sauvaire, Y., 1969. Etude avec lazote 15 de labsorption et du metabolisme
de
lammonium fourni a` concentration croissante a` des racines excisees

de mas.
Agrochimica 13, 250260.
Bieleski, R.L., 1973. Phosphate pools, phosphate transport, and phosphate availability. Ann. Rev. Plant
Physiol. 24, 225252.
Blom-Zandstra, M., Lupijn, G.L., 1987. A computer-controlled multi-titration system to study transpiration,
OHy efflux and nitrate uptake by intact lettuce plants under different environmental conditions. Plant Cell
Environ. 10, 545550.
Bloom, A.J., Sukrapanna, S.S., 1990. Effect of exposure to ammonium and transplant shock upon the
induction of nitrate absorption. Plant Physiol. 94, 8590.
Borstlap, A.C., 1981. Invalidity of the multiphasic concept of ion absorption in plants. Plant Cell Environ. 4,
189195.
Bouma, T.J., De Visser, R., 1993. Energy requirements for maintenance of ion concentrations in roots.
Physiol. Plant 89, 133142.
Breteler, H., Nissen, P., 1982. Effect of exogenous and endogenous nitrate concentration on nitrate utilization
by dwarf bean. Plant Physiol. 70, 754759.
76
Brooks, A., 1986. Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation,

photosynthetic quantum yield and amounts of some calvin-cycle metabolites in spinach leaves. Aust. J.
Plant Physiol. 13, 221237.
Brouwer, R., 1962. Distribution of dry matter in the plant. Neth. J. Agric. Sci. 10, 361376.
Brown, R.H., 1978. A difference to nitrogen use efficiency in C 3 and C 4 plants and its implication in
adaptation and evolution. Crop Sci. 18, 9398.
Brun, R., Blanc, D., 1987. Cinetique
de labsorption hydrique et minerale.
Composition ionique des solutions.
In: Blanc, D. Ed.., ATP INRA Les cultures hors-sol, INRA publications, Versailles, pp. 203220.
Brun, R., Chazelle, L., 1996. Water and nitrate absorption kinetics in the nycthemeral cycle of rose grown in
the greenhouse using a recirculating solution. J. Plant Nutr. 19, 839866.
Brun, R., Tarere, Y., Voisin, S., Saroglia, P., 1997. Cinetiques
dabsorption sur le cycle nycthemeral
de leau
et du nitrate par des plants de rosier en culture hydroponique. In: Baille, A. Ed.., Actes de lAIP Serres,
Alenya,
INRA editions,
in press.
Burns, I.G., 1990. A new method for determining critical plant concentration for maximum growth rate. In:
Scaife, A. Ed.., Proceedings of the 1st ESA Congress, European Society of Agronomy Publisher, Colmar,
Session 3 O 08.
Burns, I.G., 1994. Studies on the relationship between the growth rate of young plants and their total N
concentration using nutrient interruption techniques: theory and experiments. Ann. Bot. 74, 143157.
Burns, I.G., 1997. Interrelationships between N supply, plant N concentration and growth rate. In: Lemaire,
G., Burns, I.G. Eds.., Diagnostic Procedures for Crop N Management. colloques de lINRA, no. 82,
INRA editions,
Paris, pp. 714.
Buysse, J., Smolders, E., Merckx, R., 1996. Modelling the uptake of nitrate by a growing plant with an
adjustable root nitrate uptake capacity: I. Model description. Plant Soil 181, 1923.
Caloin, M., Yu, O., 1984. Analysis of the time course of change in nitrogen content in Dactylis glomerata L.
using a model of plant growth. Ann. Bot. 54, 6976.
Chapman, H.D., 1966. Diagnostic criteria for plants and soils. University of California, Division of Agricultural Sciences, 793 pp.
Charles-Edwards, D.A., Stutzel, H., Ferraris, R., Beech, D.F., 1987. An analysis of spatial variation in the
nitrogen content of leaves from different horizons within a canopy. Ann. Bot. 60, 421426.
Cheeseman, J.M., 1993. Plant growth modelling without integrating mechanisms. Plant Cell Environ. 16,
137147.
Claassen, N., Barber, S.A., 1974. A method for characterizing the relation between nutrient concentration and
flux into roots of intact plants. Plant Physiol. 54, 564568.
Claassen, N., Barber, S.A., 1977. Potassium influx characteristics of corn roots and interaction with N, P, Ca,
and Mg influx. Agron. J. 69, 860864.
Clarkson, D.T., 1985. Factors affecting mineral nutrient acquisition by plants. Ann. Rev. Plant Physiol. 36,
77115.
Clarkson, D.T., 1986. Regulation of the absorption and release of nitrate by plant cells: a review of current
ideas and methodology. In: Lambers, H., Neeteson, J.J., Steulen, I., Eds.., Fundamental, Ecological and
Agricultural Aspects of Nitrogen Metabolism in Higher Plants. Martinus Nijhoff Publishers, pp. 327.
Clarkson, D.T., Smith, F.W., van den Berg, P.J., 1983. Regulation of sulphate transport in a tropical legume,
Macroptilium atropurpureum cv. Siratro. J. Exp. Bot. 34, 14631483.
Clement, C.R., Hopper, M.J., Canaway, R.J., Jones, L.H.P., 1974. A system for measuring the uptake of ions
by plants from flowing solutions of controlled composition. J. Exp. Bot. 25, 8199.
Clement, C.R., Hopper, M.J., Jones, L.H.P., Leafe, E.L., 1978. The uptake of nitrate by Lolium perenne from
flowing nutrient solution. J. Exp. Bot. 29, 11731183.
Connor, D.J., Hall, A.J., Sadras, V.O., 1993. Effect of nitrogen content on the photosynthetic characteristics of
sunflower leaves. Aust. J. Plant Physiol. 20, 251263.
Cram, W.J., 1968. Compartmentation and exchange of chloride in carrot root tissue. Biochim. Biophys. Acta
163, 339353.
Cram, W.J., 1983. Chloride accumulation as a homeostatic system: set points and perturbations. The
physiological significance of influx isotherms, temperature effects and the influence of plant growth
substances. J. Exp. Bot. 34, 14841502.
77
Cromer, R.N., Kriedmann, P.E., Sands, P.J., Stewart, L.G., 1993. Leaf growth and photosynthetic response to
nitrogen and phosphorus in seedlings of Gmelina arborea. Aust. J. Plant Physiol. 20, 8398.
de Villele,
` O., 1972. Besoins en eau des cultures sous serre. Essai de conduite des arrosages en fonction de
lensoleillement. Acta Hortic. 35, 123130.
Deane-Drummond, C.E., 1986. A substrate cycling model for nitrate uptake by Pisum satium seedlings: a key
to sensitivity of response of net flux to substrate and effectors? In: Lambers, H., Neeteson, J.J., Steulen, I.
Eds.., Fundamental, Ecological and Agricultural Aspects of Nitrogen Metabolism in Higher Plants.
Martinus Nijhoff Publishers, pp. 4751.
Deane-Drummond, C.E., Glass, A.D.M., 1983. Short-term studies of nitrate uptake into barley plants using
ion-specific electrodes and 36 ClO 3 : I. Control of net uptake by NO 3 efflux. Plant Physiol. 73, 100104.
DeJong, T.M., Doyle, J.F., 1985. Seasonal relationships between leaf nitrogen content photosynthetic
capacity. and leaf canopy light exposure in peach Prunus persica.. Plant Cell Environ. 8, 701706.
Delhon, P., Gojon, A., Tillard, P., Passama, L., 1995a. Diurnal regulation of NO 3 uptake in soybean plants: I.
Changes in NO 3 influx, efflux, and N utilization in the plant during the dayrnight cycle. J. Exp. Bot. 46,
15851594.
Delhon, P., Gojon, A., Tillard, P., Passama, L., 1995b. Diurnal regulation of NO 3 uptake in soybean plants: II.
Relationship with accumulation of NO 3 and asparagine in the roots. J. Exp. Bot. 46, 15951602.
Devienne, F., Mary, B., Lamaze, T., 1994a. Nitrate transport in intact wheat roots: I. Estimation of cellular
fluxes and NO 3 distribution using compartmental analysis from data of 15 NO 3 efflux. J. Exp. Bot. 45,
667676.
Devienne, F., Mary, B., Lamaze, T., 1994b. Nitrate transport in intact wheat roots: II. Long-term effects of
NO 3 concentration in the nutrient solution on NO 3 unidirectional fluxes and distribution within the tissues.
J. Exp. Bot. 45, 677684.
Dijkshoorn, W.D., Lathwell, D.J., De Witt, C.T., 1968. Temporal changes in carboxylate content of ryegrass
with stepwise change in nutrition. Plant Soil 29, 369390.
Epstein, E., 1972. Mineral Nutrition of Plants: Principles and Perspectives. Wiley, New York.
Epstein, E., Hagen, C.E., 1952. A kinetic study of the absorption of alkali cations by barley roots. Plant
Physiol. 27, 457474.
Epstein, E., Rains, D.W., Elzam, O.E., 1963. Resolution of dual mechanisms of potassium absorption by
barley roots. Proc. Natl. Acad. Sci. 49, 684692.
Ericsson, T., Ingestad, T., 1988. Nutrition and growth of birch seedlings at varied relative phosphorus addition
rate. Physiol. Plant 72, 227235.
Evans, J.R., 1983. Nitrogen and photosynthesis in the flag leaf of wheat Triticum aestium L... Plant Physiol.
72, 297302.
Evans, J.R., 1989a. Photosynthesis and nitrogen relationships in leaves of C 3 plants. Oecologia 78, 919.
Evans, J.R., 1989b. Partitioning of nitrogen between and within leaves grown under different irradiances. Aust.
J. Plant Physiol. 16, 533548.
Evans, J.R., Farquhar, G.D., 1991. Modeling canopy photosynthesis from the biochemistry of the C 3
chloroplast. In: Boot, K.J., Loomis, R.S. Eds.., Modeling Crop PhotosynthesisFrom Biochemistry to
Canopy. CSSA special publication no. 19, American Society of Agronomy, Madison, pp. 115.
Ferrario, S., Agius, I., Morisot, A., 1992. Daily variations of xylemic exudation rate in tomato. J. Plant Nutr.
15, 6983.
Field, C., 1983. Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the
allocation program. Oecologia 56, 341347.
Field, C., Mooney, H.A., 1986. The photosynthesisnitrogen relationship in wild plants. In: Givnish, T.J.
Ed.., On the Economy of Plant Form and Function. Cambridge Univ. Press, Cambridge, pp. 2555.
Fredeen, A.L., Rao, M.I., Terry, N., 1989. Influence of phosphorus nutrition on growth and carbon partitioning
in Glycine max. Plant Physiol. 89, 225230.
Freijsen, A.H.J., De Zwart, A.J., Otten, H., 1990. A culture system for steady state nutrition in optimum and
suboptimum treatments. In: van Beusichem, M.L. Ed.., Plant NutritionPhysiology and Applications.
Kluwer Academic Publishers, Dordrecht, pp. 8185.
Gary, C., Baille, A., 1997. The carbon cycle. In. Enoch, H.Z., Stanhill, G. Eds.., Ecosystems of the World.
The Greenhouse Ecosystem. Elsevier, Amsterdam, in press.
78
Gary, C., Bertin, N., 1992. La surface specifique

foliaire comme indicateur de lequilibre
source puits chez la
tomate Lycopersicon esculentum Mill... Bull. Soc. Ecophysiol. 17, 121127.

Glass, A.D.M., Siddiqi, M.Y., 1984a. The control of nutrient uptake rates in relation to the inorganic
composition of plants. Adv. Plant Nutr. 1, 103147.
Glass, A.D.M., Siddiqi, M.Y., 1984b. Homeostats for chloride: real or apparent?. Plant Physiol. 75, S1020.
Glass, A.D.M., Siddiqi, M.Y., 1985. Nitrate inhibition of chloride influx in barley: implications for a proposed
chloride homeostat. J. Exp. Bot. 36, 556566.
Goyal, S.S., Huffaker, R.C., 1986. A novel approach and a fully automated microcomputer-based system to
study kinetics of NO 3 , NO 2 , and NH 4 transport simultaneously by intact wheat seedlings. Plant Cell
Environ. 9, 209215.
Greenwood, D.J., 1990. Production or productivity: the nitrate problem?. Ann. Appl. Biol. 117, 209231.
Greenwood, D.J., Lemaire, G., Gosse, G., Cruz, P., Draycott, A., Neeteson, J.J., 1990. Decline in percentage
N of C 3 and C 4 crops with increasing plant mass. Ann. Bot. 66, 425436.
Habib, R., Pages,
M., 1991. Approche a` lechelle
du systeme
` L., Jordan, M.O., Simonneau, T., Sebillotte,
`
racinaire de labsorption hydro-minerale.
Consequences
en matiere
Agronomie 11,
` de modelisation.
623643.
Halsted, M., Lynch, J., 1996. Phosphorus responses of C 3 and C 4 species. J. Exp. Bot. 47, 497505.
Hansen, E.M., 1972. Studies on the chemical composition of isolated soil solution and the cation absorption by
plants: I. Relationship between form and amount of added nitrogen and absorption of N, K, Na, Ca and Mg
by barley. Plant Soil 37, 589607.
Hardwick, R.C., 1987. The nitrogen content of plants and the self-thinning rule of plant ecology: a test of the
core-skin hypothesis. Ann. Bot. 60, 439446.
Hellgren, O., Ingestad, T., 1996. A comparison between methods used to control nutrient supply. J. Exp. Bot.
47, 117122.
Hirose, T., Werger, J.A., 1987a. Maximizing daily canopy photosynthesis with respect to the leaf nitrogen
allocation pattern in the canopy. Oecologia 72, 520526.
Hirose, T., Werger, J.A., 1987b. Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in
the canopy of a Solidago altissima stand. Physiol. Plant 70, 215222.
Hirose, T., Werger, J.A., Pons, T.L., van Rheenen, J.W.A., 1988. Canopy structure and leaf nitrogen
distribution in a stand of Lysimachia ulgaris L. as influenced by stand density. Oecologia 77, 145150.
Hodges, T.K., 1973. Ion absorption by plant roots. Adv. Agron. 25, 163207.
Homes,
des vegetaux.
Academie
Royale de
` M.V., van Schoor, G.H., 1982. Alimentation et fumure minerales
Belgique. Mem.
Sc. Tome 44, fascicule 3. Bruxelles.
Huguet, J.G., 1985. Appreciation
de letat
de la
hydrique dune plante a` partir des variations micrometriques
dimension des fruits ou des tiges au cours de la journee.

Agronomie 5, 733741.
Ingestad, T., Agren,

G.I., 1992. Theories and methods on plant nutrition and growth. Physiol. Plant 84,
177184.
Johnson, I.R., 1990. Plant respiration in relation to growth, maintenance, ion uptake and nitrogen assimilation.
Plant Cell Environ. 13, 319328.
Justes, E., Mary, B., Meynard, J.M., Machet, J.M., Thelier-Huches, L., 1994. Determination of a critical
nitrogen dilution curve for winter wheat crops. Ann. Bot. 74, 397407.
King, B.J., Siddiqi, M.Y., Ruth, T.J., Warner, R.L., Glass, A.D.M., 1993. Feedback regulation of nitrate influx
in barley roots by nitrate, nitrite, and ammonium. Plant Physiol. 102, 12791286.
Kochian, L.V., Lucas, W.J., 1982. Potassium transport in corn roots: I. Resolution of kinetics into a saturable
and linear component. Plant Physiol. 70, 17231731.
Kochian, L.V., Xin-zhi, J., Lucas, W.J., 1985. Potassium transport in corn roots: IV. Characterization of the
linear component. Plant Physiol. 79, 771776.
Kronzucker, H.J., Siddiqi, M.Y., Glass, A.D.M., 1995a. Kinetics of NO 3 influx in spruce. Plant Physiol. 109,
319326.
Kronzucker, H.J., Siddiqi, M.Y., Glass, A.D.M., 1995b. Compartmentation and flux characteristics of nitrate
in spruce. Planta 196, 674682.
Kronzucker, H.J., Siddiqi, M.Y., Glass, A.D.M., 1995c. Compartmentation and flux characteristics of
ammonium in spruce. Planta 196, 691698.
79
Laine,
P., Ourry, A., Macduff, J., Boucaud, J., Salette, J., 1993. Kinetic parameters of nitrate uptake by
different catch crop species: effects of low temperatures or previous nitrate starvation. Physiol. Plant 88,
8592.
Laine,
P., Ourry, A., Boucaud, J., 1995. Shoot control of nitrate uptake rates by roots of Brassica napus L.:
effects of localized nitrate supply. Planta 196, 7783.
Lambers, H., Poorter, H., 1992. Inherent variation in growth rate between higher plants: a search for
physiological causes and ecological consequences. Adv. Ecol. Res. 23, 187261.
Lambers, H., Szaniawsky, R.K., de Visser, R., 1983. Respiration for growth, maintenance and ion uptake. An
evaluation of concepts, methods, values and their significance. Physiol. Plant 58, 556563.
Larsson, C.M., 1994. Responses of the nitrate up ^take system to external nitrate availability: a whole plant
perspective. In: Roy, J., Garnier, E. Eds.., A Whole Plant Perspective on CN Interactions. SPB
Academic Publishing, The Hague, pp. 3145.
Laties, G.G., 1969. Dual mechanisms of salt uptake in relation to compartmentation and long-distance
transport. Ann. Rev. Plant Physiol. 20, 89116.
Lawlor, D.W., 1994. Relation between carbon and nitrogen assimilation, tissue composition and whole plant
function. In: Roy, J., Garnier, E. Eds.., A Whole Plant Perspective on CarbonNitrogen Interactions. SPB
Academic Publishing, The Hague, pp. 4760.
q
Le Bot, J., 1991. Diurnal uptake of NOy
by tomato plants. PhD thesis, University of Leeds, 190 pp.
3 and K
Le Bot, J., Kirkby, E.A., 1992. Diurnal uptake of nitrate and potassium during the vegetative growth of tomato
plants. J. Plant Nutr. 15, 247264.
Le Bot, J., Pilbeam, D.J., Kirkby, E.A., 1994. Plant mineral nutrition in crop production. In: Basra, A.S. Ed..,
Mechanisms of plant growth and improved productivity. Modern approaches. Marcel Dekker, New York,
pp. 3372.
Le Bot, J., Andriolo, J.L., Gary, C., Adamowicz, S., Robin, P., 1997a. Dynamique daccumulation dazote et
croissance de la tomate en hydroponie: approche de modelisation.
In: Baille, A. Ed.., Actes de lAIP
Serres, Alenya,
INRA editions,
Paris, in press.
Le Bot, J., Andriolo, J.L., Gary, C., Adamowicz, S., Robin, P., 1997b. Dynamics of N accumulation and
growth of tomato plants in hydroponics: an analysis of vegetative and fruit compartments. In: Lemaire, G.,
Burns, I.G. Eds.., Diagnostic Procedures for Crop N Management. colloques de lINRA, no. 82, INRA
editions,
Paris, pp. 3751.
Lee, R.B., 1993. Control of net uptake of nutrients by regulation of influx in barley plants recovering from
nutrient deficiency. Ann. Bot. 72, 223230.
Lee, R.B., Drew, M.C., 1986. Nitrogen-13 studies of nitrate fluxes in barley roots: II. Effect of plant N-status
on the kinetic parameters of nitrate influx. J. Exp. Bot. 37, 17681779.
Lee, R.B., Purves, J.V., Ratcliffe, R.G., Saker, L.R., 1992. Nitrogen assimilation and the control of ammonium
and nitrate absorption by maize roots. J. Exp. Bot. 43, 13851396.
Lefebvre, D.D., Glass, A.D.M., 1982. Regulation of phosphate influx in barley roots: effects of phosphate
deprivation and reduction of influx with provision of orthophosphate. Physiol. Plant 54, 199206.
Lemaire, G., Gastal, F., 1997. N uptake and distribution in plant canopies. In: Lemaire, G. Ed.., Diagnosis of
the Nitrogen Status in Crops. Springer-Verlag, Berlin, in press.
Lemaire, G., Salette, J., 1984. Croissance estivale en matiere
elevee
` seche
` de peuplements de fetuque
Festuca
arundinacea Schreb. et de dactyle Dactylis glomerata L.. dans louest de la France: I. Etude en
conditions de nutrition azotee
et dalimentation hydrique non limitantes. Agronomie 7, 381389.
Lim, J.T., Wilkerson, G.G., Raper, C.D. Jr., Gold, H.J., 1990. A dynamic growth model of vegetative soya
bean plants: structure and behaviour under varying root temperature and nitrogen concentration. J. Exp.
Bot. 41, 229241.
Lynch, J., Lauchli,
A., Epstein, E., 1991. Vegetative growth of the common bean in response to phosphorus
nutrition. Crop Sci. 31, 380387.

Maathuis, J.M., Sanders, D., 1996. Mechanisms of potassium absorption by higher plant roots. Physiol. Plant
96, 158168.
Macduff, J.H., Dhanoa, M.S., 1996. Diurnal and ultradian rhythms in K uptake by Trifolium repens under
natural light patterns: evidence for segmentation at different root temperatures. Physiol. Plant 98, 298308.
Macduff, J.H., Jackson, S.B., 1992. Influx and efflux of nitrate and ammonium in italian ryegrass and white
clover roots: comparisons between effects of darkness and defoliation. J. Exp. Bot. 43, 525535.
80
Macduff, J.H., Jarvis, S.C., Larsson, C.-M., Oscarson, P., 1993. Plant growth in relation to the supply and
uptake of NOy
3 : a comparison between relative addition rate and external concentration as driving
variables. J. Exp. Bot. 44, 14751484.
Macklon, A.E.S., Ron, M.M., Sim, A., 1990. Cortical cell fluxes of ammonium and nitrate in excised root
segments of Allium cepa L.; studies using 15 N. J. Exp. Bot. 41, 359370.
Mackown, C.T., 1987. Nitrate uptake and assimilation following nitrate deprivation. J. Exp. Bot. 38,
10791090.
Makino, A., Osmond, B., 1991. Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and
mitochondria in pea and wheat. Plant Physiol. 72, 297302.
Mankin, K.R., Fynn, R.P., 1996. Modeling individual nutrient uptake by plants: relating demand to microclimate. Agric. Syst. 50, 101114.
Marcelis, L.F.M., De Koning, A.N.M., 1995. Biomass partitioning in plants. In: Baker, J.C., Bot, G.P.A.,
Challa, H., van de Braak, N.J. Eds.., Greenhouse Climate Control: An Integrated Approach. Wageningen
Pers, Wageningen, pp. 8492.
Martin-Prevel,
P., Gagnard, J., Gautier, P., 1984. Lanalyse vegetale
dans le controle

de lalimentation des
plantes temperees
and tropicales. Technique et Documentation-Lavoisier, Paris, 810 pp.
Masle, J., Farquhar, D., Wong, S.C., 1992. Transpiration ratio and plant mineral content are related among
genotypes of a range of species. Aust. J. Plant Physiol. 19, 709721.
Mengel, K., Kirkby, E.A., 1987. Principles of Plant Nutrition, 4th edn. International Potash Institute, Bern, 687
pp.
Miller, A.J., Smith, S.J., 1996. Nitrate transport and compartmentation in cereal root cells. J. Exp. Bot. 47,
843854.
Mitscherlich, E., 1909. Das Gesetz des Minimum, das Gesetz des Abnahmenden Bodenertrages. Landw. Jahr.
38, 537552.
Mohr, H., Schopfer, P., 1995. Plant Physiology. Springer-Verlag, Berlin, 590 pp.
Morgan, M.A., Volk, R.J., Jackson, W.A., 1973. Simultaneous influx and efflux of nitrate by perennial
ryegrass. Plant Physiol. 51, 267272.
Muller,
B., Touraine, B., 1992. Inhibition of NO 3 uptake by various phloem-translocated amino acids in
soybean seedlings. J. Exp. Bot. 43, 617623.

Muschow, R.C., Sinclair, T.R., 1994. Nitrogen response of leaf photosynthesis and canopy radiation use
efficiency in field-grown maize and sorghum. Crop Sci. 34, 721727.
Nielsen, N.E., 1976. A transport kinetic concept for ion uptake by plants: III. Test of the concept by results
from water culture and pot experiments. Plant Soil 45, 659677.
Nielsen, N.E., Hansen, E.M., 1984. Macro nutrient cation uptake by plants: II. Effects of plant species,
nitrogen concentration in the plant, cation concentration, activity and activity ratio in soil solutions. Plant
Soil 77, 347365.
Nielsen, N.E., Srensen, C.B., 1984. Macro nutrient cation uptake by plants: I. Rate-determining steps in net
inflow of cations into intact and decapitated sunflower plants and intensity factors of cations in soil
solution. Plant Soil 77, 337346.
Nishio, J.N., Abadia, J., Terry, N., 1985. Chlorophyll-proteins and electron transport during iron nutritionmediated chloroplast development. Plant Physiol. 78, 296299.
Nissen, P., 1974. Uptake mechanisms: inorganic and organic. Ann. Rev. Plant Physiol. 25, 5379.
Nissen, P., 1991. Multiphasic uptake mechanisms in plants. Int. Rev. Cytol. 126, 89134.
Ourry, A., Macduff, J.H., Prudhomme, M., Boucaud, J., 1996. Diurnal variation in the simultaneous uptake
and sink allocation of NH 4 and NO 3 by Lolium perenne in flowing solution culture. J. Exp. Bot. 47,
18531863.
Pace, G.M., McClure, P.R., 1986. Comparison of nitrate uptake kinetic parameters across maize inbred lines.
J. Plant Nutr. 9, 10951111.
Papadopoulos, A.P., Liburdi, N., 1989. The Harrow fertigation manager. A computerized multifertilizer
injector. Acta Hortic. 260, 255265.
Paul, M.J., Stitt, M., 1993. Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates,
respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose. Plant
Cell Environ. 16, 10471057.
81
Pearson, C.J., Volk, R.J., Jackson, W.A., 1981. Daily changes in nitrate influx, efflux and metabolism in
maize and pearl millet. Planta 152, 319324.
Peuke, A.D., Kaiser, W.M., 1996. VI. Nitrate or ammonium uptake and transport, and rapid regulation of
nitrate reduction in higher plants. In: Behnke, H.D., Luttge,
U., Esser, K., Kadereit, J.W., Runge, M.
Eds.., Progress in Botany, Vol. 57. Springer-Verlag, Berlin, pp. 93113.

Pitman, M.G., 1971. Uptake and transport of ions in barley roots: I. Estimation of chloride fluxes in cells of
excised roots. Austr. J. Biol. Sci. 27, 407421.
Ran, Y., Habib, R., Bar-Yosef, B., Erez, A., 1994. Root volume effects on nitrogen uptake and partitioning in
peach trees. Agron. J. 86, 530534.
Rao, K.P., Rains, D.W., 1976. Nitrate absorption by barley: I. Kinetics and energetics. Plant Physiol. 57,
5558.
Reynolds, J.F., Chen, J., 1996. Plant Soil. Modelling whole-plant allocation in relation to carbon and nitrogen
supply. Coordination versus optimization: opinion. Plant Soil 185, 6574.
Robinson, D., 1994. The responses of plants to non-uniform supplies of nutrients. New Phytol. 127, 635674.
Rufty, T.W. Jr., Huber, S.C., 1983. Changes in starch formation and activities of sucrose phosphate synthase
and cytoplasmic fructose 1.6 bisphosphatase in response to sourcesink alterations. Plant Physiol. 72,
474480.
Rufty, T.W. Jr., Huber, S.C., Volk, R.J., 1988. Alterations in leaf carbohydrate metabolism in response to
nitrogen stress. Plant Physiol. 88, 725730.
Sage, R.F., Pearcy, R.W., 1987a. The nitrogen use efficiency of C 3 and C 4 plants: I. Leaf nitrogen, growth,
and biomass partitioning in Chenopodium album L.. and Amaranthus retroflexus L... Plant Physiol. 84,
954958.
Sage, R.F., Pearcy, R.W., 1987b. The nitrogen use efficiency of C 3 and C 4 plants: II. Leaf nitrogen effects on
the gas exchange characteristics of Chenopodium album L.. and Amaranthus retroflexus L... Plant
Physiol. 84, 959963.
Sanders, F.E., 1993. Modelling plant growth responses to vesicular arbuscular mycorrhizal infection. Adv.
Phytopathol. 9, 135166.
Scaife, A., 1989. A pumprleakrbuffer model for plant nitrate uptake. Plant Soil 114, 139141.
Schacht, H., Schenk, M.K., 1990. Control of nitrogen supply of cucumber Cucumis satius . grown in soilless
culture. In: van Beusichem, M.L. Ed.., Plant NutritionPhysiology and Application. Kluwer Academic
Publishers, Dordrecht, pp. 753758.
Schenk, M.K., 1996. Regulation of nitrogen uptake on the whole plant level. Plant Soil 181, 131137.
Siddiqi, M.Y., Glass, A.D.M., 1982. Simultaneous consideration of tissue and substrate potassium concentration in Kq uptake kinetics: a model. Plant Physiol. 69, 283285.
Siddiqi, M.Y., Glass, A.D.M., 1986. A model for the regulation of Kq influx, and tissue potassium
concentrations by negative feedback effects upon plasmalemma influx. Plant Physiol. 81, 17.
Siddiqi, M.Y., Glass, A.D.M., 1987. Regulation of Kq influx in barley: evidence for a direct control of influx
by Kq concentration of root cells. J. Exp. Bot. 38, 935947.
Siddiqi, M.Y., Glass, A.D.M., Ruth, T.J., Rufty, T.F., 1990. Studies of the uptake of nitrate in barley: I.
Kinetics of 13 NO 3 influx. Plant Physiol. 93, 14261432.
Siddiqi, M.Y., Glass, A.D.M., Ruth, T.J., 1991. Studies of the uptake of nitrate in barley: III. Compartmentation of NO 3 . J. Exp. Bot. 42, 14551463.
Silberbush, M., Barber, S.A., 1983. Sensitivity of simulated phosphorus uptake to parameters used by a
mechanistic mathematical model. Plant Soil 74, 93100.
Sinclair, T.R., Horie, T., 1989. Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop
Sci. 29, 9098.
Smart, J., Garvin, D.F., Prince, J.P., Lucas, W.J., Kochian, L.V., 1996. The molecular basis of potassium
nutrition in plants. Plant Soil 187, 8189.
Suniaga Quijada, J., 1991. Nutrition azotee
de la tomate de type determine,
issue de semis. Analyse de la

croissance et du developpement
au stade jeune. These
` de Doctorat, Universite de Rennes I, 173 pp.

Sylvester-Bradley, R., Stokes, D.T., Scott, R.K., Willington, V.B.A., 1990. A physiological analysis of the
diminishing responses of winter wheat to applied nitrogen: II. Evidence. Asp. Appl. Biol. 25, 289300.
Tanner, W., Beevers, H., 1990. Does transpiration have an essential function in long-distance ion transport in
plants?. Plant Cell Environ. 13, 745750.
82
Teyker, R.H., Jackson, W.A., Volk, R.J., Moll, R.H., 1988. Exogenous 15 NO 3 influx and endogenous 14 NO 3
efflux by two maize Zea mays L.. inbreds during nitrogen deprivation. Plant Physiol. 86, 778781.
Thornley, J.H.M., 1972. A balanced quantitative model for root: shoot ratios in vegetative plants. Ann. Bot.
36, 431441.
Thornley, J.H.M., 1995. Shoot: root allocation with respect to C, N and P: an investigation and comparison of
resistance and teleonomic models. Ann. Bot. 75, 391405.
Touraine, B., Muller, B., Grignon, C., 1992. Effect of phloem-translocated malate on NO 3 uptake by roots of
intact soybean plants. Plant Physiol. 99, 11181123.
Touraine, B., Clarkson, D.T., Muller, B., 1994. Regulation of nitrate uptake at the whole plant level. In: Roy,
J., Garnier, E. Eds.., A Whole Plant Perspective on CN Interactions. SPB Academic Publishing, The
Hague, pp. 1130.
Tribo-Blondel,
A.M., 1979. Dynamique comparee
de labsorption des nitrates et de leau par des plantules de

ble.
C.R. Acad. Sci. Paris Ser.
D 288, 15451548.
Ulrich, A., 1952. Physiological bases for assessing the nutritional requirements of plants. Ann. Rev. Plant
Physiol. 3, 207228.
van der Werf, A., Kooiman, A., Welschen, R., Lambers, H., 1988. Respiratory energy costs for the
maintenance of biomass, for growth and for ion uptake in roots of Carex diandra and Carex acutiformis.
Physiol. Plant 72, 483491.
van Noordwijk, M., 1990. Synchronisation of supply and demand is necessary to increase efficiency of
nutrient use in soilless culture. In: van Beusichem, M.L. Ed.., Plant NutritionPhysiology and Application. Kluwer Academic Publishers, Dordrecht, pp. 525531.
Vessey, J.K., Layzell, D.B., 1987. Regulation of assimilate partitioning in soybean. Initial effects following
change in nitrate supply. Plant Physiol. 83, 341348.
Veen, B.W., 1980. Energy cost of ion transport. In: Rains, D.W., Valentine, R.C., Hollaender, A. Eds..,
Genetic Engineering of Osmoregulation. Impact on Plant Productivity for Food, Chemical and Energy.
Plenum, New York, pp. 187195.
von Liebig, J., 1841. The organic chemistry and its application on agriculture and physiology. Verlag
Viehweg, Braunschweig, 167 pp.
Wang, M.Y., Siddiqi, M.Y., Ruth, T.J., Glass, A.D.M., 1993a. Ammonium uptake by rice roots: I. Fluxes and
subcellular distribution of 13 NH 4 . Plant Physiol. 103, 12491258.
Wang, M.Y., Siddiqi, M.Y., Ruth, T.J., Glass, A.D.M., 1993b. Ammonium uptake by rice roots: II. Kinetics of
13
NH 4 influx across the plasmalemma. Plant Physiol. 103, 12591267.
Wikstrom,
G.I., 1995. The relationship between the growth rate of young plants and their total N
F., Agren,
concentration is unique and simple: a comment. Ann. Bot. 75, 541544.
Wild, A., Jones, L.H.P., Macduff, J.H., 1987. Uptake of mineral nutrients and crop growth: the use of flowing
nutrient solutions. Adv. Agron. 41, 171219.
Willits, D.H., Nelson, P.V., Peet, M.M., Depa, M.A., Kuehny, J.S., 1992. Modeling nutrient uptake in
Chrysanthemum as a function of growth rate. J. Am. Hortic. Sci. 117, 769774.
Wong, S., Cowan, I.R., Farquhar, G.D., 1985. Leaf conductance in relation to rate of CO 2 assimilation: I.
Influence of nitrogen nutrition, phosphorus nutrition, photon flux density and ambient partial pressure of
CO 2 during ontogeny. Plant Physiol. 78, 821825.

Modelling Nutrition

Hochgeladen von

Dokumentinformationen

Copyright

Verfügbare Formate

Dieses Dokument teilen

Dokument teilen oder einbetten

Freigabeoptionen

Stufen Sie dieses Dokument als nützlich ein?

Sind diese Inhalte unangemessen?

Copyright:

Verfügbare Formate

Modelling Nutrition

Hochgeladen von

Copyright:

Verfügbare Formate

Scientia Horticulturae 74 1998.

Modelling plant nutrition of horticultural crops:

Corresponding author. E-mail: lebot@avignon.inra.fr

0304-4238r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved.

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

4. Operational approach of nutrition . . . . . . . . . . . . . . . . .

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

Agronomists and plant physiologists have developed a dual approach to characterize

Growth: final yield

dose of one element

rate of supply of one element relative addition rate m.

thermodynamic activity ratio

solution ion content

plant and solution contents

HqrOHy excretion NO 3 , NH 4 and

von Liebig 1841.

1992.; Larsson 1994.

Siddiqi and Glass 1982.; Cram 1983.

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

Dijkshoorn et al. 1968.; Ben Zioni et al. 1971.

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

Epstein and Hagen 1952.

Epstein et al. 1963.

Kochian and Lucas 1982.

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

PO42y, SO42y, NOy

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

Influx minus efflux E .

Claassen and Barber 1974.

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

Siddiqi and Glass 1982, 1986.

error actuated feedback on Im

error actuated feedback on Im

Buysse et al. 1996.

From a mechanistic viewpoint, a direct negative feedback of internal potassium and

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

under optimum temperature and humidity conditions at ambient CO 2 levels. Similarly,

A x s maximum A max , as constant, N0 s N at zero A max

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

2. A max could be regulated independently from nitrogen by stomata, CO 2 diffusion

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

but could result either from 1. an underestimation of A max or 2. a decrease in CO 2

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

for review, see Ingestad and Agren,

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

vary according to plant species Agren,

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

These findings may be interpreted as an indication that under non-limiting nitrogen

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

therefore, total nitrogen concentration n. is:

that is, N A W 0.66

According to Hardwick 1987., for a given species, there is a curvilinear relationship

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

4. Operational approach of nutrition

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

J. Le Bot et al.r Scientia Horticulturae 74 (1998) 4782

However, EC measurement is partially relevant to the system since it provides only