REVIEW

New Phytol. (2000), 147, 155169

Research Review

Kinetics of nutrient uptake by roots :

responses to global change
HORMOZ BASSIRIRAD
Department of Biological Sciences, University of Illinois at Chicago,
845 West Taylor Street, Chicago, IL 60607, USA (tel j1 312 996 8674 ;
fax j1 312 413 2435 ; e-mail hormoz!uic.edu)
Received 7 December 1999 : accepted 24 March 2000

There is a growing recognition that accurate predictions of plant and ecosystem responses to global change require
a better understanding of the mechanisms that control acquisition of growth-limiting resources. One such key
mechanism is root physiological capacity to acquire nutrients. Changes in kinetics of root nitrogen (N) uptake
might influence the extent to which terrestrial ecosystems will be able to sequester excesses in carbon (C) and N
loads. Despite its significant role in determining plant and ecosystem cycling of C and N, there is little information
on whether, or how, root nutrient uptake responds to global change. In this review various components of global
change, namely increased CO concentration, increased soil temperature and increased atmospheric N deposition
#
and their effects on kinetics of root nutrient uptake are examined. The response of root nutrient uptake kinetics
to high CO is highly variable. Most of this variability might be attributable to differences in experimental
#
protocols, but more recent evidence suggests that kinetic responses to high CO are also species-specific. This
#
raises the possibility that elevated CO might alter community composition by shifting the competitive interaction
#
of co-occurring species. Uptake of NH + and NO seem to be differentially sensitive to high CO , which could
%
$
#
influence ecosystem trajectory toward N saturation. Increased soil temperature might increase N and P uptake
capacity to a greater extent in species from warm and fluctuating soil habitats than in species from cold and stable
soil environments. The few available data also indicate that increased soil temperature elicits a differential effect
on uptake of NH + versus NO . Root uptake kinetics are generally down-regulated in response to long-term
%
$
exposure to atmospheric N deposition. The extent of this down-regulation might, however, vary among species,
stages of succession, land-use history and plant demand. Nonetheless, it is suggested that root N uptake kinetics
might be an accurate biological indicator of the ecosystem capacity to retain N. The results reviewed here clearly
highlight the scanty nature of the literature in the area of root nutrient absorption responses to global change. It
is also clear that effects of one component of global change on root nutrient absorption capacity might be
counterbalanced by another. Therefore, the generalizations offered here must be viewed with caution and more
effort should be directed to rigorously test these initial observations in future research.
Key words : global change, elevated CO , root nutrient uptake kinetics, soil temperature, atmospheric nitrogen
#
deposition.

Whole-plant response to global atmospheric change

is the product of a complex set of processes that
results from coordinated interactions between root
and shoot (Farrar & Jones, 2000). As the main organ
involved in water and nutrient uptake and as one of
the major sinks for assimilated C, roots play a critical
role in determining plant and ecosystem responses to
various facets of global change ranging from N
deposition and elevated CO (Norby, 1998 ; Van
#
Noordwijk et al., 1998) to elevated ozone and UV-B
(Pell et al., 1995 ; Klironomos & Allen, 1995 ;
Rennenberg et al., 1996 ; Scagel & Andersen, 1997 ;
Whitfield et al., 1998). Despite the growing rec-

ognition that roots play a critical role in determining

the overall response of terrestrial vegetation to global
change, very little is known about the mechanisms
involved.
An important rootshoot interaction that might
determine the overall response of plants is the ability
of the root system to adjust nutrient acquisition
capacity to meet variations in shoot demand caused
by environmental changes. Plant roots can alter their
nutrient acquisition capacity by adjusting their
physiological, longevity, morphological and\or
architectural characteristics to meet changes in shoot
nutrient demand (Chapin, 1980 ; Clarkson &
Hanson, 1980 ; Clarkson, 1985). Even though
physiological capacity of root nutrient uptake is only

156

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H. BassiriRad

CO2
Plant nutrient
demand

Shoot
growth

Nutrient-use
efficiency

CH2O

Carbohydrates or
photoassimilates

Photosynthesis
&
transpiration

Soil temperature & N

deposition

Root
compensatory adjustments
Symbiotic association
e.g. mycorrhizas and N2 fixation
Uptake kinetics
Turnover & life span

Plant
nutrient uptake

Nutrient availability at the

root surface
Decomposition & mineralization
Mass flow
Diffusion

Water flux

Fig. 1. A conceptual diagram depicting the way in which kinetics of root nutrient uptake, together with various
other factors, can influence availability and uptake of nutrients in response to elevated CO concentration,
#
increased soil temperature and atmospheric N deposition. The diagram also shows that changes in other root
characteristics, for example growth, morphology, architecture, life span and mycorrhizal association, might
counterbalance and\or obviate adjustments in kientics that would otherwise be elicited.

one of the number of adjustments that influences

nutrient acquisition, its response to changes in plant
environment might provide a key mechanistic explanation of why some species are more sensitive to
global change than others. However, it should be
highlighted that the degree to which kinetics of
nutrient uptake or other potential adjustments are
expressed would ultimately depend on soil nutrient
availability and soil factors that determine nutrient
transport to the root surface (Fig. 1).
Studies of shoot responses to global change
commonly examine physiological parameters such as
photosynthetic rate and stomatal conductance. By
contrast, studies of root responses to global change
often focus on root growth and morphological
characteristics, seldom addressing changes in physiological characteristics such as hydraulic conductivity
and kinetics of ion uptake. Active root nutrient
absorption is a highly adaptive plant characteristic
that influences acquisition of N and other nutrients
in response to environmental factors (Chapin, 1980 ;
Forde & Clarkson, 1999). Therefore, knowledge of
changes in the kinetics of nutrient uptake and the
relative species differences is critical in predicting
ecosystem responses to global change. Although in
recent years a number of investigators have underscored the need for a better understanding of how,
for example, elevated CO changes root uptake
#

kinetics (Norby, 1994 ; Rogers et al., 1994 ; Luo et

al., 1999), there has been relatively little response to
this plea. This is surprising particularly when one
considers that, at least in the short-term, physiological adjustments are less costly to the plant and
more likely to act as a primary signal that leads to
longer term responses in root morphology and
architecture.
This review will first introduce the relevant
concepts, definitions and measurement techniques
related to root ion transport systems. This background will be drawn upon in the later sections to
offer possible explanations of the high degree of
variability in uptake kinetic responses particularly to
high CO concentrations. The review will then
#
examine adjustments in nutrient uptake kinetic
responses to three components of global change ;
elevated atmospheric CO concentration, increased
#
anthropogenic N deposition and higher soil
temperature. The main focus of the review is
on root physiological adjustments associated with
the uptake of N ; however, whenever possible, the
uptake of other nutrients will also be addressed.
Furthermore, because elevated CO , N deposition
#
and higher soil temperature are likely to occur
concurrently, the paper will also consider the
potential interactive effects of these factors on root
ion absorption.

REVIEW

Nutrient uptake kinetics and global change

: ,

Root uptake kinetics : the transporter concept and
definitions
Ions typically move across the root into the xylem by
traversing several layers of plasmalemma. Ion movement across the cell membrane is highly sensitive to
changes in soil or root temperature (Chapin, 1974 ;
BassiriRad et al., 1993), oxygen concentration of the
rooting medium (Epstein, 1972), metabolic inhibitors (Glass & Siddiqi, 1995), and light and\or
carbohydrate availability (Rufty et al., 1984 ; Glass,
1989 ; Raper et al., 1991), which strongly suggest the
presence of an energy-dependent uptake system.
Despite the early recognition by Van den Honert
(see Glass, 1989) that root ion uptake is an active
process, a clear mechanism of uptake was not put
forward until Epstein & Hagen (1952) introduced
the concept of membrane-bound transporters or
carriers.
Much of the evidence for this hypothesis came
from the similarity in the behavior of ion uptake
versus external ion concentration and that of
enzyme activity versus substrate concentration (i.e.
rate of root ion uptake increases with increasing ion
concentration until a saturation kinetics is reached
beyond which uptake rate is independent of ion
concentration). According to this mechanism, transporters are membrane-bound proteins that exhibit a
high degree of specificity for individual ions in much
the same way enzymes do for a specific substrate.
Because of this analogy, Epstein suggested that
similar to enzyme-substrate relationships, the
carrier-mediated transport across the root can be
similarly described by the MichaelisMenten model :
v l Vmax[c]\(Kmj[c])
(c is the concentration of an individual ion whose
uptake rate, v, is controlled by uptake capacity, Vmax,
when all available carriers are occupied, and by the
apparent affinity of the transporters, Km.)
Subsequent work by Epstein (1976) as well as
numerous others (Van den Honert & Hooymans,
1955 ; Becking, 1956 ; Lycklama, 1963 ; Behl et al.,
1988 ; Pilbeam & Kirkby, 1990 ; Glass & Siddiqi,
1995) has established that net uptake of most of the
essential ions, including NH + and NO , can be
%
$
described by the MichaelisMenten model. This
model can adequately describe the uptake of NH +
%
and NO at external concentrations below 100200
$
M. At these relatively low substrate concentrations,
the uptake of NO is controlled by a single
$
transporter-mediated system known as the high
affinity transport system (HATS). However, uptake
at external concentrations
200 M is not consistent
with a single transport system. This is apparently
because of the presence of additional transport

157

systems that operate at relatively high external ion

concentrations. For example, three transport systems
have been identified for NO uptake in plant roots
$
exposed to concentrations of 01000 M. The first
two systems display a saturable behavior whereas the
third one is linear (Glass & Siddiqi, 1995 ; von Wiren
et al., 1997). The second saturable transport system
and the linear system are known as low affinity
transporter systems (LATS) and have a significant
contribution to the overall uptake at relatively high
ion concentrations. Uptake of NH + has also been
%
shown to display multiphasic transporter characteristics where HATS dominates uptake at low
external concentrations while a nonsaturable LATS
dominates uptake at relatively high NH + con%
centrations (Glass & Siddiqi, 1995 ; von Wiren et al.,
1997). An alternative view was proposed by Nissen
(1971) and Nissen & Martin-Nieto (1998) who
suggested that the multiphasic nature of transport
systems can be explained by a single transporter
system which undergoes a concentration-dependent
phase change. However, recent cloning of different
genes encoding for HATS and LATS (Forde &
Clarkson, 1999) is inconsistent with a single transporter hypothesis.
Because LATS is operative only at high substrate
concentrations, the relative contribution of this
system to the overall nutrient acquisition of the plant
might increase where roots are likely to encounter
patches and pulses of high nutrient availability. In
most ecologically relevant circumstances, however,
bulk soil solution concentration is so low that the
relative contribution of the LATS becomes negligible. Therefore, in addressing nutrient uptake in a
changing environment the most meaningful component of the root nutrient uptake system is the HATS
and its kinetics parameters.

Measurements of net ion uptake kinetics

There are a number of methods that allow estimations of the kinetic parameters for nutrient
uptake. These techniques often determine net ion
uptake, which is a function of both influx and efflux.
A more detailed account of these methods is given in
BassiriRad et al. (1999). Briefly, these methods
involve direct measurements of uptake rate from a
range of external ion concentrations using either
excised or intact roots. When excised roots are used,
uptake from a bathing medium, containing tracers
such as "&N or $#P, is estimated from accumulation
of the tracers in the root tissues. In the intact root
techniques, usually a depletion approach is used
which might or might not involve the use of a tracer.
Commonly, these methods yield measurements of
net uptake rate from a range of ion concentrations
enabling estimations of kinetic parameters. A number of studies presented in this review determine

158

REVIEW

H. BassiriRad

rates of uptake from a single concentration that

represents the maximum velocity of uptake, or
uptake capacity, Vmax. This practice is analogous to
gas exchange studies where only Amax (maximum
photosynthetic rates) are determined at saturating
light. Although these single point data do not provide
a complete picture of the changes in kinetic behavior,
they provide an indication of whether the uptake
capacity of the system has been altered in relative
terms.

Responses to high CO
#
It is commonly accepted that an important determinant of plant and ecosystem responses to
elevated CO concentrations is plant nutrient status
#
(Eamus & Jarvis, 1989 ; Bazzaz, 1990 ; Lloyd &
Farquhar, 1996). Therefore, knowledge of root
characteristics that influence nutrient uptake and
their response to elevated CO concentrations is
#
critical in accurately predicting the long-term plant
and ecosystem responses to CO enrichment. A
#
number of recent reviews have examined CO #
induced changes in root characteristics, for example,
growth and morphology (Tingey et al., 2000) and
mycorrhizal association (Treseder & Allen, 2000)
that should influence nutrient uptake. Here, the way
in which elevated CO might alter root nutrient
#
uptake kinetics is examined.
Two distinct yet related principles motivated the
early predictions of how active root ion uptake
should respond to high CO . First, elevated CO , at
#
#
least in the short-term, has been shown to accelerate
growth. Higher growth rate should then increase
plant nutrient demand and uptake capacity (Lee,
1982 ; Clarkson, 1985). Second, models of wholeplant C nutrient balance (Bloom et al., 1985 ;
Johnson, 1985 ; Robinson, 1986 ; Luo et al., 1994 ;
Gutschick & Kay, 1995) predict that resources of
abundant availability (C), must be allocated to
increase the uptake of the most limiting resource
(nutrients). A large number of CO studies have
#
demonstrated both a short-term stimulation of
growth and increased supply of root respiratory
substrates (Cruz et al., 1993 ; Tschaplinski et al.,
1993). Yet data on root uptake kinetics show no
consistent pattern of uptake response to high CO .
#
The first direct measurements of root uptake
responses to CO enrichment were reported by
#
Newbery et al. (1995) who examined the rates of N,
phosphorus (P) and potassium (K) uptake in Agrostis
capallaris, at three different external concentrations,
and found no significant CO effect. Using field
#
grown loblolly pine saplings that had been exposed

to 18 months of CO treatment, BassiriRad et al.

#
(1996b) found no significant changes in Vmax of NH +
%
uptake, but elevated CO significantly enhanced Vmax
#
for NO uptake. Jackson & Reynolds (1996) also
$
found no effect of elevated CO on NH + uptake
#
%
rates of six grassland annuals, but NO uptake rate
$
was inhibited in response to CO enrichment. Other
#
studies listed in Table 1 have also produced equally
inconsistent patterns. Even in cases where similar
species are examined, effect of CO on kinetics of
#
NH + varies from one experiment to the next
%
(BassiriRad et al., 1996a,b).
The observed variability in root nutrient uptake
responses to high CO is consistent with the
#
variability observed in many other plant parameters
that have been examined under high CO . Tingey et
#
al. (2000) underscored a high degree of variability in
root growth responses to high CO . Similarly,
#
analysis of shoot growth responses from a number of
field CO experiments exhibits a high degree of
#
variability (Norby et al., 1999). It now appears that,
with the exception of a few important plant characteristics, for example, water-use efficiency, photosynthetic rate, tissue N concentration and nonstructural carbohydrates, most plant processes are
extremely variable in response to high CO (Luo et
#
al., 1999). The most obvious drawback of such a
high degree of variability is that our ability to predict
plant responses to high CO will remain limited until
#
the underlying mechanisms that cause this variability
are understood.
In that regard, the most important question is : to
what extent can the observed variability in nutrient
uptake responses be attributed to differences in
experimental protocols ? Experiments vary considerably from one laboratory to another in terms
of : growth conditions particularly soil water and
nutrient availability ; duration of the CO treatment ;
#
uptake assay method (e.g. using an excised root
technique versus an intact root system, or using an
uptake assay solution which contains NH + and
%
NO singly or in combination) ; the range of external
$
ion concentrations at which the kinetics parameters
are determined (i.e. some experiments might use a
range that includes only the HATS whereas others
might use a range which includes both the HATS
and the LATS) ; and stages of development. An
example of how differences in experimental protocol
can lead to a different pattern of uptake response was
highlighted by BassiriRad et al. (1996a,b) where
elevated CO was shown to downregulate uptake
#
kinetics of NH + in one experiment (BassiriRad et
%
al., 1996a) but had no significant effect on the
kinetics of NH + uptake in another experiment
%
(BassiriRad et al., 1996b) even though the same
species, loblolly pine, was used in both. The two
experimental protocols differed in many respects
including length of the growing season, use of pot
versus field grown plants, length of the CO
#

REVIEW

Nutrient uptake kinetics and global change

159

Table 1. Responses of root NO and NH + uptake capacity and whole-plant growth to elevated CO
$
%
#
Uptake rates
Species

NH +
%

NO
$

Growth

Reference

Acer saccharum
A. rubrum
Glycine max
Sorghum bicolor
Avena fatua
Bromus hordeaceus
Lolium multiflorum
Vulpia microstachys
Lasthenia californica
Plantago erecta
Mixed-species community
Ceratonia siliqua
Agrostis capillaris
Pinus taeda
P. ponderosa
P. taeda
P. ponderosa
P. taeda
Bouteloua eriopoda
Prosopis glandulosa
Larrea tridentata
Populus tremuloides

nc
Increase
nc
nc
nc
nc
nc
nc
nc
nc
nc
nc
nc
Decrease
Decrease
nc
Decrease
nc
nd
nd
nd
nc

nc
nc
nc
nc
nc
Decrease
nc
nc
Decrease
Decrease
nc
nc
nd
nd
nd
Increase
Increase
Increase
Increase
nc
Decrease
nc

nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
nd
Increase
nc
Increase
Increase
Increase
Increase
nd
Increase
Increase
Increase
Increase

BassiriRad et al. (1999)

BassiriRad et al. (1999)
BassiriRad et al. (1999)
BassiriRad et al. (1999)
Jackson & Reynolds (1996)
Jackson & Reynolds (1996)
Jackson & Reynolds (1996)
Jackson & Reynolds (1996)
Jackson & Reynolds (1996)
Jackson & Reynolds (1996)
Jackson & Reynolds (1996)
Cruz et al. (1993)
Newbery et al. (1995)
BassiriRad et al. (1996a)
BassiriRad et al. (1996a)
BassiriRad et al. (1996b)
BassiriRad et al. (1997a)
BassiriRad et al. (1997a)
BassiriRad et al. (1997b)
BassiriRad et al. (1997b)
BassiriRad et al. (1997b)
Rothstein et al. (2000)

nc, no change ; nd, not determined. Growth is measured as changes in total dry mass of the plants.

exposure, seedlings versus saplings, and plants

grown with NH + as the sole source of N versus
%
those receiving both NH + and NO . Therefore, in
%
$
the search for a pattern, comparing such studies will
not be very fruitful unless possible interactions of
these experimental differences and CO are ruled
#
out.
However, the possibility remains that, even after
accounting for experimental differences, a large
source of variation in uptake responses to high CO
#
can be explained only by species differences. Regardless of the plant process being examined,
interspecies differences have a far-reaching ecological significance and must be examined cautiously.
Recently, Norby et al. (1999) reviewed tree responses
to CO enrichment and concluded that a commonly
#
invoked explanation for differences in response
variables to high CO is that species respond
#
differently . They warned against the use of species
differences as an explanation unless the confounding
effects of experimental conditions have been ruled
out. Recently, Zerihun & BassiriRad (2000) examined NH + and NO uptake kinetic responses of
%
$
six broad-leaf and conifer tree species grown under
identical conditions and found that root NH + uptake
%
kinetic responses to high CO are clearly species#
dependent. Whenever possible, similar effort (e.g. to
standardize experimental conditions) should be
employed to rule out unequivocally the differences
caused by environmental factors. Alternatively,

evaluation of species differences should be limited to

experiments that are directly comparable. However,
only a limited number of CO studies have examined
#
nutrient uptake kinetics, thereby making such a task
very difficult. Therefore, it is necessary to generate
more data in this area before reliable assessments can
be made.
Notwithstanding the limited data, interspecies
differences in uptake kinetics under high CO might
#
have important consequences for plant and ecosystem responses. Interspecific variation in root
physiological characteristics might explain why some
species do not exhibit a commonly observed decline
in tissue nutrient concentration at high CO . In a
#
study of three desert species, BassiriRad et al.
(1997b) showed that elevated CO decreased foliar N
#
and P concentration in Larrea tridentata and Prosopis
glandulosa, but not in Bouteloua eriopoda, which was
the only species that had upregulated its root uptake
rate for both N and P. Species-specific responses of
N uptake kinetics could also be one of the potential
mechanisms by which elevated CO might affect
#
competitive balance among co-ocurring species,
thereby affecting ecosystem productivity and composition (Berntson et al., 1998).
In considering the effects of high CO on root N
#
absorption other complexities must also be considered. Plant N is primarily supplied from the
available soil NO and NH + solution, but the
$
%
relative preference for each form might largely

160

REVIEW

H. BassiriRad

depend on the ability of roots to absorb, assimilate

and translocate that form. Although uptake and
assimilation of both N forms require expenditure of
energy, considerably more energy is associated with
the uptake and assimilation of NO than of NH +,
$
%
largely because NO must be metabolically reduced
$
to ammonia before it can be assimilated (Haynes &
Goh, 1978 ; Blacquie' re, 1987). The respiratory cost
of uptake and assimilation of NH + can be as little as
%
half that for the uptake and assimilation of NO
$
(Bloom et al., 1992). Therefore, when the rate of
carbohydrate supply to the root, and hence its energy
production, is limiting, NO is a less favorable N
$
form (Turpin et al., 1985). Studies that have
measured root N uptake capacity commonly report a
differential effect of elevated CO on NH + versus
#
%
NO (BassiriRad et al., 1996b). Surprisingly, how$
ever, in some cases elevated CO has an inhibitory
#
effect on root NO uptake capacity (Jackson &
$
Reynolds, 1996). In the case of NO uptake species
$
differences in responses to elevated CO might
#
represent differences in the predominant site of
NO reduction. Nitrate can be assimilated in root
$
and shoot or both and the assimilation rate is directly
correlated with NO uptake (Pate, 1973 ; Smirnoff
$
& Stewart, 1985 ; Andrews, 1986). Under optimal
light conditions, shoot NO might be photo$
assimilated with very little demand for carbohydrates
whereas root assimilation is almost exclusively
dependent on respiratory energy supplied by carbohydrates (Pate & Layzell, 1990 ; Sechley et al., 1992).
Whether the projected rise in atmospheric CO
#
concentration would disproportionately benefit
NO uptake in root-versus shoot-reducing species
$
remains unknown.
Obviously, research in the area of root nutrient
uptake responses to high CO is still in an embryonic
#
stage and more data needs to be generated before
generalizations can be made. More importantly,
however, the challenge still remains of whether a
specific pattern of response in kinetics of nutrient
uptake can be used as a predictive tool in assessing
whole-plant and ecosystem responses to high CO .
#
As highlighted in Table 1, even in cases where
kinetics of uptake are severely down-regulated, the
overall plant growth response to CO is still positive.
#
This is partly because root uptake kinetic response is
only one potential mechanism that can lead to
changes in nutrient uptake. As illustrated in the
conceptual model (Fig. 1), adequate changes in other
root compensatory characteristics such as morphology and life span, along with increased nutrientuse efficiency, can prevent the need for a positive
adjustment in the kinetics of uptake. Furthermore,
positive adjustments in uptake kinetics under high
CO might also be unnecessary if availability of
#
nutrients increased either because of increased
mineralization or atmospheric deposition (Fig. 1).
Jackson & Reynolds (1996) examined root physio-

logical uptake capacity for N and root-biomass

responses of a mixed community of annual grasses
and forbs. They reported that N-uptake responses to
elevated CO were more closely correlated with root
#
physiological capacity under low N availability, but
correlated more strongly with root biomass under
relatively high N availability.
A. Zerihun et al. (unpublished) showed that the
relative contribution of root physiological uptake
capacity in determining the overall plant responses
to CO enrichment must be evaluated in conjunction
#
with other root mechanisms (Fig. 1) that can also
influence nutrient acquisition. Ultimately, plant
nutrient acquisition in an elevated CO environment
#
will be regulated by the interaction of compensatory
adjustments in root growth, lifespan, physiology and
symbiotic association. Therefore, future studies
addressing the relative contribution of active ion
uptake to plant nutrient status and growth responses
to high CO will require experimental designs that
#
monitor changes in these mechanisms simultaneously. A number of recent studies emphasized
the need for such an integrated approach (Berntson
& Bazzaz, 1996, 1997, 1998), but none has directly
measured root nutrient uptake rate.

Responses to soil temperature

It is estimated that the temperature of the globe
might rise by as much as 24mC during the twentyfirst century (Houghton, 1991), increasing mean soil
temperature in many terrestrial ecosystems. Such
changes will have a marked effect on soil biology
including growth and physiological characteristics of
roots. Soil temperature has long been considered as
an important ecological factor that determines a
variety of structural and functional characteristics in
managed and natural ecosystems (Chapin, 1974 ;
Rykbost et al., 1975 ; Dixon & Turner, 1991 ;
Farnsworth et al., 1995 ; Chapin, 1977 ; Weih &
Karlsson, 1999). In some ecosystems, temperature
of the root zone is the most important factor in
determining net primary productivity (Van Cleve et
al., 1981 ; Risser, 1985). In addition, as a major
factor determining the length of the growing season,
soil temperature influences community composition
and\or structure (Black & Bliss, 1980 ; Van Cleve et
al., 1981, 1990 ; Farnsworth et al., 1995 ; Harte &
Shaw, 1995 ; Thompson & Naeem, 1996).
A number of potential mechanisms might be
responsible for this tight control of ecosystem
properties by soil temperatures. The most notable
are the direct effects of soil temperature on biogeochemical processes that regulate N and water
availability in the soil (Pastor & Post, 1988 ;
Bouwman, 1990 ; Mellilo et al., 1990 ; Parsons et al.,
1994 ; Zak et al., 1999). Soil thermal regime has a
dramatic effect on root growth and morphology (Gill

REVIEW

Nutrient uptake kinetics and global change

& Jackson, 2000 ; Pregitzer et al., 2000) as well as

root respiration (Atkin et al., 2000). Van Cleve et al.
(1990) found that in Picea mariana, soil warming
improved foliar N, P and K status, but because root
characteristics were not measured, an exact mechanism was not offered. However, others have shown
that soil warming might negatively effect root
characteristics such as growth, morphology and
longevity (Anderson & McNaughton, 1973 ;
Hendrick & Pregitzer, 1993 ; Redmond, 1995).
Improved plant nutrient status when root growth
and morphological characteristics are negatively
affected raises the possibility that soil warming
might increase plant nutrient acquisition by enhancing root uptake kinetics.
Indeed, a number of studies have demonstrated
that changes in soil temperature can directly effect
plant nutrient acquisition by changing root transport
properties for NH + (Chapin et al., 1986), NO
%
$
(Cumbus & Nye, 1982 ; BassiriRad et al., 1991,
1993), PO $ (Chapin, 1974, 1977 ; Cumbus & Nye,
%
1985), and K+ (Siddiqi et al., 1984). The exact
mechanism for temperature-induced changes in
nutrient uptake capacity is not clearly understood.
Temperature sensitive processes, such as root respiration, which mediate ion movement across the
root, can partially explain the observed changes in
nutrient uptake with increasing soil temperature. In
fact, the Q for the uptake of many ionic species (i.e.
"!
PO $, K+ and NH +) is between 2 and 3, cor%
%
responding to similar Q values for root respiration
"!
(Glass, 1989). However, ion uptake is not the only
root function that requires energy supply from
respiration. Other important metabolic processes
(i.e. root growth and maintenance) also represent
energetic cost that must be met by respiration.
Therefore temperature-induced changes in root
respiration should not be used as a direct surrogate
for estimating changes in nutrient uptake. This point
was highlighted by the work of Bravo-F & Uribe
(1981) who demonstrated that in corn roots, absorption rates for P and K reached a maximum at 25
and 35mC, respectively, whereas root respiration did
not reach its optimum even at 40mC. In addition,
they found that the Q for respiration was two- to
"!
threefold smaller than those for P and K uptake at
temperature ranges 22mC but the Q values were
"!
similar at temperature ranges
22mC. These observations stress that Q data obtained in a narrow
"!
range of soil temperatures cannot be linearly scaled
up to a wider temperature range, a point that has also
been made with respect to root respiration (Atkin et
al., 2000).
Root-zone temperature might also affect nutrient
absorption capacity by changing fluidity of the fatty
acids in root plasmalemma (Clarkson et al., 1988).
Much of the evidence for this proposed mechanism
has come from observing a sharp break in the
Arrhenius plots of uptake versus the inverse of root

161

temperature (Clarkson & Warner, 1979 ; Markhart et

al., 1979 ; Bravo-F. & Uribe, 1981). In fact, on the
basis of such an approach critical temperatures have
been proposed for different ionic species. Clarkson &
Warner (1979) demonstrated that this break occurred at a markedly higher root temperature for
NO uptake than for NH + uptake (14 and 9mC,
$
%
respectively). Most plant species, especially trees,
have a distinct preference for NH + rather than NO
%
$
when both N forms are simultaneously present in the
rooting medium. However, this preference is further
enhanced if soil temperature drops to
10mC
(Marschner et al., 1991 ; Glass & Siddiqi, 1995 ;
Gessler et al., 1998). Therefore, it follows that plant
species that are likely to experience higher soil
temperatures are likely to show a greater relative
preference for NO than for NH + (Table 2). This
$
%
might have significant implications in ecosystems
that are currently experiencing chronic atmospheric
N deposition largely in the form of NO . If soil
$
temperature and NO availability in these systems
$
increase simultaneously, vegetation uptake capacity
might be much higher than currently believed and
might explain why the onset of N saturation is
delayed.
A few studies have shown that the temperature
sensitivity of NO uptake capacity is highly
$
modulated by the N status of the roots or the whole
plant. For example, BassiriRad et al. (1993)
examined effects of soil temperature in a field-grown
tussock grass, Eriophorum vaginatum. In plants that
were grown with supplemental N, soil temperature
had no significant effect on root Vmax for NO
$
uptake, but in plants that received no supplemental
N, uptake capacity was significantly higher at soil
temperatures of 17mC than at 27mC. Working with a
number of catch crop species, Laine! et al. (1993) also
observed a high sensitivity of the NO uptake
$
capacity in response to changes in root-zone temperature in N-starved, but not in N-supplied plants.
The modulation of root ion uptake responses to soil
temperature by plant N status has been interpreted
by some investigators as a possible explanation for an
internal compensation that would override any direct
effects of temperature. In fact, Clarkson et al. (1988)
suggested that the response of nutrient uptake to
temperature might represent changes in plant nutrient demand per unit root and not an acclimatory
change in root transport properties. According to
this, the degree to which soil temperature might alter
nutrient uptake capacity is largely determined by the
degree to which growth and root : shoot ratio is
affected (Fig. 1). If changes in soil temperature lead
to an increased root-absorbing surface relative to
shoot size, then there will be a down-regulation of
ion influx. On the other hand, if changes in soil
temperature lead to a relative increase in shoot
versus root size, then ion uptake is likely to increase
per unit root. Again, these observations highlight an

162

REVIEW

H. BassiriRad

Table 2. Differential effects of changes in soil or root temperature on NH + and NO uptake rate in various
%
$
species
Species
Lolium multiflorum

Brasica napus

Picea abies
Lycopersicon esculentum
Chilling sensitive
Chilling resistant
Ceratina siliqua
N-fed seedlings
N-depleted seedlings

Picea abies

Fagus sylvatica

Soil or root
temperature (mC)

NH + : NO
$
%
uptake ratio

References

5
10
20
5
9
17
10
20

3n20
2n50
1n60
1n87
1n20
0n87
5n00
4n20

Clarkson & Warner

(1979)

5
20
5
20

1n10
0n69
0n90
0n76

Smart & Bloom (1991)

10
22
30
10
22
30
10
20
25
10
20
25

1n90
1n13
1n06
1n70
1n30
1n00
31n0
17n5
10n0
9n00
3n10
3n80

MacDuff et al. (1987)

Marschner et al. (1991)

Cruz et al. (1993)

Gessler et al. (1998)

The effect is shown as changes in the ratio of NH + to NO uptake rates, which are often expressed on a root dry weight
%
$
basis.

earlier conclusion that kinetics of root nutrient

uptake and its relative importance to plant nutrient
acquisition must be viewed in conjunction with
other compensatory factors (Fig. 1) whose responses
might counterbalance that of the kinetics.
Although evidence suggests that nutrient uptake
capacity generally increases in response to soil
warming (Gosselin & Trudel, 1986) caution must be
exercised in generalizing such an effect across a
broad range of species and soil temperatures. For
example, Chapin et al. (1986) reported enhanced
uptake kinetics for NH + in several taiga tree species
%
when root temperature was increased from 10 to
20mC. BassiriRad et al. (1996c) also found that
increase in soil temperature from 5 to 15mC significantly increased kinetics of root PO $ uptake in
%
Eriophorum vaginatum, a tundra species, but a
further increase from 15 to 25mC significantly
inhibited rates of root PO $ absorption. In his early
%
work with root P uptake capacity, Chapin (1974,
1977) postulated that the degree of root response to
soil temperature changes is determined by the soil
thermal characteristics of the habitat of origin. He
showed that species from thermally stable cold soil
environments were significantly less sensitive to a

shift in soil temperature than their counterparts

from habitats with warmer and more fluctuating soil
environments. This differential sensitivity of species
to changes in soil temperature based on thermal
regimes of the habitat of origin is consistent with
differences observed in their fatty-acid composition
(Pike & Berry, 1980).

Summary and potential interaction with elevated

CO
#
In general, increased soil temperature appears to
have a more consistent effect on root nutrient uptake
kinetics than elevated CO . It is not known whether
#
elevated CO and higher soil temperature will have
#
an interactive effect on root nutrient uptake kinetics.
Furthermore, a modest increase in soil temperature
is likely to enhance root nutrient absorption capacity,
but it is uncertain if such an increase is sufficient to
meet increased nutrient demand under high CO
#
concentrations. In Eriophrum vaginatum, increase in
soil temperature from 5 to 15mC increased PO $
%
uptake capacity to the same extent in ambient and
high-CO plants (BassiriRad et al., 1996c). However,
#

REVIEW

Nutrient uptake kinetics and global change

high-CO plants had a significantly lower P con#

centration regardless of the soil temperature, indicating that warmer soils did not enhance uptake
enough to prevent the commonly observed drop in
tissue P concentration in response to high CO . Soil
#
thermal characteristics of the habitat of origin might
also be an important factor. Increased soil temperature might have a greater impact on root nutrient
uptake of plants adapted to warm and fluctuating soil
thermal regimes than on those adapted to cold but
stable thermal environments. Although higher soil
temperatures might, in general, increase root N
uptake capacity, it seems plausible that uptake of
NO rather than NH + might be more responsive to
$
%
such an increase. Like soil temperature, elevated
CO has been shown to elicit a differential effect on
#
root NH + and NO uptake rates, but the pattern
%
$
and universality of those responses remain equivocal.
Finally, estimates of potential effects of soil warming
on root nutrient uptake capacity based on indirect
methods must proceed with extreme caution. For
example, despite a tight linkage between root
nutrient uptake and respiration, it should not be
assumed that increased soil temperature would affect
root nutrient uptake as a linear function of root
respiration.

Responses to N deposition
Another important component of global change that
will significantly effect terrestrial and aquatic ecosystems is the chronic deposition of atmospheric N
(Lovett, 1994 ; Galloway et al., 1995 ; Vitouseck et
al., 1997 ; Norby, 1998). The rate of increase in
atmospheric N deposition during the last three
decades has far surpassed that of atmospheric CO
#
concentration (Vitousek et al., 1997). Although many
ecosystems are N-limited, and should theoretically
respond positively to this increase, there are many
uncertainties associated with long-term consequences of atmospheric N deposition. For example, several models proposed an increase in C
storage capacity of the northern temperate forest
ecosystems in response to N deposition (Melillo &
Gosz, 1983 ; Peterson & Melillo, 1985 ; Schimel,
1995 ; Townsend et al., 1996). More recently,
however, it has been argued that the actual increase
in C storage in many of these ecosystems due to
enhanced atmospheric N input is considerably less
than previously thought (Norby, 1998 ; Nadlehoffer
et al., 1999b).
Similarly, other models of ecosystem responses to
atmospheric N deposition, for example, the N
saturation model of Aber et al. (1989), have been
recently re-evaluated (Aber et al., 1998). In its initial
version, the N saturation model predicted that,
particularly in forest areas where NO rather than
$
NH + dominates the deposition, N input would
%

163

exceed the retention capacity of the system. Once the

system has reached this critical N load a cascade of
events, including changes in soil pH and cationic
balance, would follow that are deleterious to tree
species (Aber et al., 1989 ; Schulze, 1989). The need
to re-evaluate the N saturation model was, in part,
motivated by the observation that the sensitivity of
ecosystems to N deposition is highly variable (Aber
et al., 1998). For example, addition of N for 6 yr at
the rate of 90 g m# did not induce any symptoms of
saturation in a pine stand in the Harvard Forest
(MA, USA). By contrast, an addition rate of only
15 g m# was enough to induce symptoms of N
saturation in a stand of spruce-fir in Mt. Ascutney
(NH, USA ; Magill et al., 1996). The differential
ecosystem sensitivities observed in N-loading experiments were attributed to differences in land-use
history, but might result from differences in retention capacity of these systems (Norby, 1998).
Together these factors determine how far each
system is from being N-saturated. Therefore, a more
reliable prediction of the ecosystem response to N
deposition requires a better understanding of the
factors that determine biological uptake capacity of
the system.
Biological control of ecosystem N retention
depends on both microbial immobilization and on
the uptake capacity of the vegetation. In some
ecosystems, microbial immobilization, including
mycorrhizal uptake, is the primary mechanism that
incorporates atmospheric N input into soil organic
matter (Johnson, 1992 ; Nadelhoffer et al., 1995,
1999a ; Aber et al., 1998). Hanson et al. (1994)
suggested that excessive NO losses in a riparian
$
ecosystem undergoing a simulated N saturation were
moderated by increased rate of N storage into soil
organic matter, and denitrification. However, as
already stated, the capacity of a system to retain
deposited N will also be determined by the vegetation and its capacity to absorb soil N. Increased
plant capacity to absorb NO might, in part, explain
$
why in a number of recent N addition experiments,
N retention was considerably greater than expected
(Aber et al., 1998).
Nadelhoffer (2000) addressed fine-root turnover
in response to N deposition. Unfortunately, very few
data are available on whether, and how, root N
uptake capacity responds to high atmospheric N
deposition. In general, N addition down-regulates
root N uptake capacity (Chapin, 1980 ; Clarkson &
Hanson, 1980 ; Clarkson, 1985 ; Glass, 1989), but the
extent of this response might depend largely on plant
N demand (Forde & Clarkson, 1999). If N availability is limiting growth, then atmospheric N
deposition is expected to enhance uptake until
growth demand for N is met. Beyond this point,
however, further N addition will either be accompanied by no change in root N absorption
capacity or will reduce it. Kinetics of root N uptake

164

REVIEW

H. BassiriRad

and its response to N addition can vary considerably

among species (Lee & Rudge, 1986 ; Glass, 1989)
often showing a strong correlation with the growth
rate of the species (Garnier et al., 1989 ; Lambers &
Poorter, 1992 ; Schenk, 1996). At early successional
stages, the community is dominated by fast-growing
species with relatively high capacity for NO versus
$
NH + absorption (Chapin et al., 1986). Conversely,
%
late-successional forest communities are dominated
by species such as spruce that have low root NO
$
uptake capacity (Kronzucker, et al., 1995, 1996).
Cautiously interpreted, these observations indicate
that fast-growing species with a higher uptake
capacity might be better able to dampen the
deleterious effects of N deposition than slowgrowing plants that have a characteristically low N
uptake rate. Tree species commonly have a greater
capacity for NH + than NO uptake (Chapin et al.,
%
$
1986 ; Gessler et al., 1998 ; Wallenda & Read, 1999),
but conifers are even less capable of taking up NO
$
than broad-leaf species (BassiriRad et al., 1997a ;
Kronzucker et al., 1997). Therefore, systems that are
dominated by conifers and other species that can
meet their N demand from NH + uptake, are less
%
likely to reduce the negative effects of NO
$
deposition on forests ecosystems.
Because plants are still considered as critical
modifiers of the N saturation process (Aber et al.,
1998), there has been a growing interest in developing a strong plant indicator that might accurately
assess plant capacity to retain N and the degree of
ecosystem N saturation. Possible indicators are foliar
N analysis and ratios of other elements to N (Cape et
al., 1990 ; Bauer et al., 1997 ; Aber et al., 1998).
Although total leaf N status is an indicator of plant
N demand, it does not always predict plant capacity
to absorb additional N. Rather, root capacity to
absorb NO and NH + is more closely associated
$
%
with specific pools of N, for example, root cytoplasmic concentration of NO , NH +, or specific
$
%
amino acids such as glutamine and aspargine (Lee &
Drew, 1986 ; Siddiqi et al., 1990 ; Cousin & Barneix,
1993). In addition, interpretation of foliar N can be
confounded if NO and NH deposition intercepted
#
$
and absorbed by the leaf is translocated to the root
where it elicits a feedback inhibition of uptake
(Rennenberg & Gessler, 1999). Finally, foliar analysis is a diagnostic that cannot accurately predict any
changes in relative preference of plants for NH +
%
versus NO . Therefore, it is suggested that direct
$
measurements of root uptake capacity might be a
stronger indicator of plant capacity to retain N.
A few laboratories have already used root N
uptake as a measure of plant N status or N demand.
Jones et al. (1991) and Jones & Dighton (1993)
showed a negative correlation between root uptake
rate and high leaf N status and suggested that root
uptake capacity can be used as a bioassay of plant N
status. Rates of root NH + uptake in Pinus sylvestris
%

from northern Sweden were reduced by almost fourfold in plants that had been fertilized by additional N
compared with untreated control plants, in just one
growing season (Jones et al., 1994). Rothstein et al.
(1996) examined changes in NO uptake kinetics of
$
two field- and laboratory-grown maple species in
response to NO amendment and found no changes
$
in root NO uptake kinetics (Table 3). They
$
suggested that these species would not act as a
significant sink for NO . In a relatively com$
prehensive study, Ho$ gberg et al. (1998), measured
root NO and NH + uptake capacities for a number
$
%
of forest species in a cross-national transect from
northern Sweden to southern France. This study
included a number of forest trees and an N
deposition gradient that ranged from a low of 1 kg
ha" yr" at a site in Sweden to 27 kg ha" yr" at a site
in southern France. Higher N deposition (which at
these sites are dominated by NO ) was inversely
$
correlated with NH + uptake rate. This could explain
%
the inhibitory effects of N deposition on NH +
%
uptake since high root N concentration has been
implicated as a feedback controller of N uptake
(Siddiqi et al., 1990). However, like Rothstein et al.
(1996), this group found a very insignificant NO
$
uptake rate by the dominant species tested and this
rate was unaffected by NO addition rate or fine
$
root N concentration.
Summary and potential interaction with high CO
#
and soil temperature
Models designed to predict the potential impact of
chronic atmospheric N deposition require a better
understanding of biological capacity to retain N and
how that capacity might change with the projected
rise in atmospheric N deposition. The availability of
N at the root surface is determined by factors such as
the rate of N deposition, mineralization, mass flow
and diffusion in the soil (Nye & Tinker, 1977).
However, root transporters involved in the uptake of
NH + and NO ultimately regulate N entry into the
%
$
plant. The few available data indicate that root N
uptake capacity generally decreases in response to
long-term exposure to N deposition (Table 3). The
onset and the extent of this inhibition, however,
might depend on species, plant demand as set by
either N status of the plant or relative growth rate,
land use history, successional stage and the effects
interacting of other components of global change
with N deposition. Regardless of these modifiers,
measurements of root N uptake kinetics, combined
with information about total active root surfaces
(Nadelhoffer, 2000), can offer an accurate diagnostic
tool to assess whether vegetation can absorb the
additional N load should that N become available at
the root surface. In addressing the possible effects of
N addition on root uptake kinetics the potential
interaction of other components of global change

REVIEW

Nutrient uptake kinetics and global change

165

Table 3. Effects of N-deposition and\or addition rates on NH + and NO uptake rates

%
$
Uptake rate
( mol g" h")
Species

Site

Pinus sylvestris

Umea/ , Sweden

Acer saccharum

Michigan, USA
A
B
C
D

Pinus taeda

North Carolina, USA

Populus tremuloides

Michigan, USA

Betula spp.
P. sylvestris
Picea abies
P. abies
Fagus sylvatica
P. abies
F. sylvatica
P. abies

A/ heden, Sweden

Klosterhede, Denmark
Aubure, France
Schacht, Germany
Waldstein, Germany

N-deposition rate
(kg ha" yr")
5
37
74
103

NH +
%
1n55
0n64
0n36
0n35

4
34
6
36
8
38
8
38
Ambient
Ambientj200
*
**
1
1
1
27
6
6
16
20

27n9
19n1
13n4
7n4
7n1
4n6
8n1
7
2n1
4n7
3n40
1n92

NO
$

References

Jones et al. (1994)

0n56
0n23
0n65
0n70
0n45
0n43
1n02
1n24
4n3
3n0
0n52
0n17
0n25
0n23
1n33
0n23
0n06
0n40
0n60
0n16

Rothstein et al. (1996)

BassiriRad et al. (1996b)

Rothstein et al. (2000)
Ho$ gberg et al. (1998)

Uptake rates were determined from solutions that contained NH + and NO at or near-saturating concentrations hence
%
$
they represent Vmax. All studies were conducted in the field but only the study by Ho$ gbert et al. (1998) represents
unmanipulated gradient of N-deposition. * and ** represent control (unsupplemented) and fertilized plots with net N
mineralization rate of 0n434 g N g" soil wk", and 2n26 g N g" soil wk", respectively. The study by Rothstein et al.
(1996) was conducted at four different hardwood forest sites in Michigan designated by authors as A, B, C and D.

must also be considered. It has already been noted

that soil warming might stimulate root N uptake rate
particularly when N is available as NO . In
$
addition, elevated CO might also enhance rates of
#
NO uptake without a significant effect on the
$
uptake of NH + (BassiriRad et al., 1996b). Increases
%
in availability of C and N should theoretically affect
rates of N uptake by plant roots. However, these
factors might affect uptake in different directions.
Field-grown saplings of both loblolly pine
(BassiriRad et al., 1996b) and Populus tremuloides
(Rothstein et al., 2000) showed a marked downregulation of NH + and NO uptake capacity in
%
$
response to N addition regardless of the growth
CO concentration. Taken together these data
#
suggest that the pattern of response in root N uptake
kinetics might be more strongly regulated by N
deposition than the elevated atmospheric CO con#
centration.

A number of soil and plant factors regulate nutrient

acquisition by plants. Models designed to predict

plant and ecosystem responses to global change

require a better understanding of these factors.
Although mineralization, bulk soil solution concentration, mass flow and diffusion are the overriding
factors determining nutrient, particularly N, availability at the root surface, nutrient intake into the
plant is largely determined by root physiological
uptake capacity. Despite this, root nutrient uptake
kinetic response to the various components of global
change is not commonly investigated. Obviously,
there is urgent need to generate more data in this
area to improve prediction of long-term plant
responses to the projected changes in the global
environment. To this end, it is suggested that future
studies of plant responses to global change should
more frequently integrate measurements of root
nutrient absorption into the study design. Also
highlighted is the fact that root nutrient uptake
kinetics do not respond similarly to different aspects
of global change. For example, long-term exposure
to high N deposition decreases N uptake capacity
whereas soil warming enhances it. This suggests that
the overall responses of root absorption capacity
might not be entirely appreciated unless the counter-

166

REVIEW

H. BassiriRad

acting effects of various components of global

change are considered. Finally, adjustment in uptake
kinetics is only one of a number of potential rootlevel mechanisms that could enable plants to meet
changes in shoot demand. Other potential mechanisms such as increased biomass allocation to fine
active roots, changes in morphology and architecture
and a higher degree of mycorrhizal infection must be
considered together with kinetics of root nutrient
uptake.

I wish to thank Jacqueline Charette for her assistance in
the preparation of this manuscript. Thanks also to Diana
Lane, Ayalsew Zerihun, John Constable and John
Lussenhop who provided critical reviews of an earlier
version of the manuscript. Special thanks to Glen Berntson
and an anonymous reviewer who also provided helpful
comments and suggestions. This work was funded by the
United State Department of Energy contract no. DEFG02-97ER62332 and the National Science Foundation
grant no. IBN-9728785.

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