Factors Affecting Mineral Nutrient Acquisition Plants: Further

ANNUAL
REVIEWS Further
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Ann. Rev. Plant Physiol. 1985.36:77-115
Copyright © 1985 by Annual Reviews Inc. All rights reserved
FACTORS AFFECTING
MINERAL NUTRIENT
Annu. Rev. Plant. Physiol. 1985.36:77-115. Downloaded from www.annualreviews.org
ACQUISITION BY PLANTS
Access provided by 103.215.210.235 on 12/11/21. For personal use only.
David T. Clarkson
Letcombe Laboratory, Wantage, aXI2 9JT, United Kingdom
CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
PROPERTIES OF THE ROOT SURFACE ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ... . . . 78
I dentification of the Most I mportant Propertie sfro m Mathe matical Mo dels ofNutrient
Upta ke fro m Soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
Root Hairs . . . . . . . . . . . . ............................................ ................... .............. 82
Mo dification of Rhizosphere Nutrient Availability by Plant Roots . . . . . . . . . . . . . . . . . ...... 85
MYCORRHIZAS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
Signi ficant Nutrient Upta ke into the Host . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
Fungal Infection an d Phosphate Nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
Manipulation of Host -Fungus Association .... . . . . ...... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
REGULATION OF NUTRIENT INTAKE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
Short-ter m Mo dulation Relate d to Internal Concentration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
Longer -term A djustment of Carrier Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
Regulation by Efflu x Control ... ....... . . . . . .... . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
Flu xes Through the Sy mplast . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98
The Si ze of the Absorbing S Ulface . . .......................... .. ............... ............ .... 98
Conclusions . . . . . . . . . ............ ................................................................... 99
THE ENERGY COST OF MINERAL NUTRITION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
Broa d Sense Costs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
Narrow Sense Costs . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
CONCLUDING REMARKS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
INTRODUCTION
The word acquisition emphasizes that more is involved in getting inorganic

nutrients into plants than ion transport across cell membranes.
77
0066-4294/85/0601 -0077$02.00
78 CLARKSON
The present review is concerned with two interfaces; much of the subject
matter relates to events occurring at OI very near the root/soil interface, and the
review itself attempts to provide an interface between plant physiology and soil
science. Even at the risk of having rocks thrown from both sides, I suggest that
many of the intriguing processes that occur in the root/soil interface merit a
more purposeful and integrated investigation, especially by plant physiolo
gists, than they have received. From a vast amount of published work I have
been very selective in choosing matters that raise interesting physiological
questions. I have not dealt with dinitrogen fixation by nodule-forming organ
isms or by free-living N-fixing microorganisms since these vigorous fields are

frequently reviewed; neither have I attempted to detail the various influences of
environment on nutrient acquisition. The discussion opens with results of

mathematical modeling which suggest the relative importance of root prop
erties in nutrient acquisition; the more important properties are then examined.
It is widely known that many plants are unable to acquire enough phosphorus
from unfertilized soils or to forage effectively for other nutrients without the
assistance of mycorrhizas. The discussion here deals with the nutrient ex
changes between host and fungus in vesicular-arbuscular mycorrhizas (VAM)
and the energetic "cost" of maintaining the association. Growth is the pacemak
er for nutricnt inflow to the plant, and this inflow can be regulated by varying
the relative size of the absorbing system or the capacity of its uptake mechan
isms. There is considerable diversity in the way that different types of plants
manage their affairs when confronted by growth-limiting supplies of mineral
nutrients (29). The last major section of this chapter concerns the consumption
of energy in nutrient acquisition. In summary,this review asks what factors are
of the greatest importance in nutrient acquisition, how is it regulated, and what
does it cost?
PROPERTIES OF THE ROOT SURFACE

Identification of the Most Important Properties from
Mathematical Models of Nutrient Uptake from Soil
Most models that describe processes involved in nutrient uptake by roots in soil
integrate values for root size (usually length) and its increase with time,nutrient
inflow into the roots as related to nutrient concentration in the soil solution near
the root surface (this incorporates both kinetic and plant demand factors), and
nutrient transport in the soil by convection or diffusion. Increasingly elaborate
models have been developed which show that, given sensible values for input
parameters, such matters as microbial interception of nutrients in the rhizo
sphere (56) and age-dependent factors relating to the physiology of roots (57)
can be modeled. It is difficult for a nonmathematician to comment on the
correctness of these models, but it is plain to everyone that the input data
MINERAL NUTRIENT ACQUISITION 79
involve guesswork in most cases. The models tell us what we could predict if
we knew more about the rhizosphere than we do. All models indicate that root
growth and extension into unexploited volumes of soil are of great significance
in acquiring nutrients that diffuse slowly in the soil ( 1 42). Actual observation
and computer simulation show that root geometry is of minor significance in
the interception of mobile nutrients such as sulphate (78) or nitrate and ammo
nium (161).
Competition between roots depends on their density in the soil (usually
expressed as length of root per unit volume of soil) and the pattern of their
distribution. The latter is a laborious matter to determine and very difficult

where the roots of more than one species are being considered. From a
theoretical standpoint at least (7), both density and pattern influence predictions
of nutrient uptake from soil. Roots compete with one another for mobile
nutrients such as sulphate or nitrate at much lower densities than they compete
for P and Zn and perhaps K because the radius of the zone of soil from which
roots extract ions is much greater in the former instances and hence depletion
shells come to overlap one another (142). Models that make no allowance for
root competition [e.g. Claassen & Barber (34)] greatly overestimate the uptake
of more mobile nutrients such as K, while giving reasonable fits for P uptake
(169). Models that accommodate root density (55) give better, but still not
exact, fits for K+ uptake by soybeans in commercially fertilized soil (174).
Parameters for root dispersion can be added to models easily enough, but the
notional values used to bring the model into line with observed uptake may or
may not have any relation to what actually occurs in the soil.
Modeling such complex processes as soillrhizosphere/root interactions has
been most impressive and useful, but experimental verification of the models
has usually been conducted in soil with high levels of mineral amendment.
Thus, in some of the experiments discussed below, [PiJ soil solution was raised
to between 14 and 50 f.LM, i.e. ten- to fifty-fold greater than might be expected
in fertile natural soils. As is shown in sensitivity analyses of models (101, 175),
root growth rate and initial soil solution concentration have very large effects
on the predicted values for P uptake (Figure 1). In such circumstances there is
little constraint on plant growth by nutrient supply, and other considerations
would lead us to expect that parameters which measure plant growth would be
of overriding significance. The predictive powers of models for phosphate
uptake deteriorate where nutrient concentrations are low; it is then that ilI
defined factors which determine the "efficiency" of absorption become impor
tant.
KINETIC PARAMETERS OF ION ABSORPTION In several models kinetic pa

rameters for ion absorption by solution-grown plants were used to estimate
nutrient inflows into roots growing in soil. Depletion of labeled nutrients from
80 CLARKSON
0'5
k
0-4
&
......
C/)
Q)
"0 De
E
E
0-3
w
::.c::
;5
a..
Imax
::::) Vo
a.. r1
Cmin
0-2 Km
0·1
��--�----�--��-�
0·5 1-0 1-5 2·0
CHANGE RAT IO
Figure 1 Effects of changing parameter values on computed phosphorus uptake by pot-grown
soybeans ( 1 75). Predicted P uptake in this nutrient-rich soil was well correlated with measurements
using parameter values equivalent to I on the change ratio scale. The predicted value is highly
sensitive to increases or decreases in rate of root elongation (k), root diameter (ro), and the initial
soil solution concentration (Cl,). while soil parameters such as diffusion coefficient (De) and buffer
power (b) have greater effects if their values are diminished than if they are increased. Ion uptake
properties of the root (km• Imax> Cmin) have relatively little effect on the predicted uptake. and
transpiration (measured via Vol is without effect. The spacing between roots (rtl was wide [the
initial value of ri was ten times greater than that at which inter-root competition for P is likely
( 142)]. and hence there was no effect caused by changing this value. Lines passing through the
cross have been omitted for clarity.
solutions follows a Michaelis-Menten relationship and can be used to derive

values for Imax (equivalent to VmaJ and Km (70, 140). The net inflow In at a
given nutrient concentration at the root surface can be calculated.
== Imax (Cs - Cmin)

Km + (Cs - C m in)
where I max is the maximal inflow at high (saturating) levels of Cs

Cs == concentration at root surface

Cmin ==concentration at which there is no net inflow, i. e. In == °

Km = Cs-Cmin where In V2/max·
=
This application of ion transport kinetics must have encouraged public

spirited laboratory workers to believe that their painstaking observations were
actually useful in the real world. When cultivars of barley differing from one
another in either Imax or Km were grown in a soil of moderate P-deficiency, the
most evident correlations found were between phosphate uptake from the soil
and root length,but a model incorporating the kinetic parameters predicted the
uptake by different variety quite well (141). Several facts about kinetic parame
ters seem to have been overlooked in the enthusiasm generated in this work. In
a given cultivar, I max and/or Km are likely to vary with plant age (24, 204, 207),
the nutrient concentration to which the plant has been acclimatized (81, 207),
and the nutrient status of the plant (38a,39,69,80,118). In addition,Imax may
be directly dependent on the inherent vigor of a plant (23, 29, 31) and vary
inversely with the relative root size or the fraction of root having access to the
nutrient (118). A sensitivity analysis on the predictions of the Cushman (55)
model for P uptake by soybeans (Figure 1) shows how little the outcome is
influenced by variations of the kinetic parameters for uptake by the root. Given
the errors inherent in modeling and measurement, it scarcely seems to matter
what values are used, and this explains why values determined in circum
stances radically different from those in soil could be applied with apparent
success. Greater affinity of the transport system or greater capacity,as reflected
by Imax, would both be of great significance in the absorption of nutrients from
dilute solutions (118). Many plants appear to do one or sometimes both of these
things as a first response to nutrient deficiency, suggesting that the kinetic
parameters are important in nutrient-poor surroundings. Effective selection of
crop varieties for life in soils of lower fertility takes this factor into account (83,
141, 172).
ROOT EXTENSION The sensitivity analysis in Figure 1 shows root growth rate
( = extension) to have the greatest influence on the phosphate extracted from a
82 CLARKSON
given volume of soil. Root growth rate measures two things: it is a measure of
the "demand" created by plant growth, and it measures the rate at which they
enter unexploited volumes of soil where relatively high concentrations of
phosphate and other nutrients are found. The analysis suggests that the initial
rate of absorption by apical zones of roots from solution concentrations, which
may nearly saturate [max, may account for most of the phosphate intake
necessary to sustain growth. This suggestion is supported by the strong influ
ence of the initial soil solution concentration. Root diametcr (r0) is also among
the sensitive factors; the most effective way in which species can vary root
diameter is by the development of root hairs.

Root Hairs
GEOMETRICAL CONSIDERATIONS Root hairs represent a way of increasing
the root radius and thus expanding the absorbing surface for a modest invest
ment of dry matter. In theory at least, each hair will absorb nutrient ions in its
immediate vicinity, but the frequency of hairs is often large so that hairs will
begin to compete with one another; their "depletion" shells quickly overlap and
the whole length of the root hair may be situated in "exhausted" soil. At this
point the effective boundary of the root is described by a circle drawn around
the tips of the root hairs (14). This view of root hairs and their soil environment
does not take into account the actual sequence of events that leads to their
development. The root hairs emerge and elongate in a zone several millimeters
behind the root tip in most species. The cells of the root apex and elongation
zone will have had the opportunity to absorb P for several hours before the hairs
begin to emerge, and the concentration of P in the solution at the root surface
will have fallen already to a low level compared with the bulk soil. The
depletion shell around the root is, in other words, close to being formed before
the root hairs emerge, particularly if [Pi] in the bulk soil is low. From theoretical
considerations of the soil solution concentration and diffusion coefficient, the
width of the depletion shell can be calculated; for phosphate its outer limit
usually lies between 100 to 200 J.Lm from the root surface. Root hairs that are
shorter than this can be expected to have relatively little impact on absorption
since they develop in "exhausted" soil. It is only where root hairs extend
beyond the depletion shell created by the root epidermal surface that they will
have access to the bulk soil solution concentration of a nutrient. These predic
tions were largely borne out in experimental observations on seven species
differing in root hair length and frequency (102) and in a sensitivity analysis of
a model developed to take account of root hairs on phosphate absorption (101).
The species used had root hair: root surface area ratios varying between 0.2 for
Allium cepa and 3.8 for Salsola kali (Russian Thistle). The latter species had a
relatively low density, 89 mm-1, of long hairs, 0.6 mm, on slender roots
(average radius 0.056 mm)-a combination predicted to maximize the efficien-
cy of the absorbing system for phosphate. The root hair length and frequency in
Zea mays and Loliumperenne also seem to have this combination (153). One of
the benefits of such a geometrical arrangement is that dry matter investment to
produce a large root surface is small. In Salsola kali only 16% of plant dry
weight was in roots whereas in wheat, which had shorter hairs (0.29 mm) on
thicker roots (average radius 0.11 mm), 34% of the plant dry weight was in the
roots. A similar point about root hairs and fine branching minimizing the root
dry weight/unit soil needed to maintain optimal N uptake rate (as either N03- or
NH4 + ) emerges from the model of Robinson & Rorison (161).
ROOT HAIR DEVELOPMENT Several questions about the physiology and

development of root hairs are raised by the work above. What factors determine
root hair density and length? To what extent can length and density vary? Do
root hairs have a functional lifetime and, if so, is this determined in a practical
sense by the availability of nutrients or does it depend on structural modifica
tion as hairs get older? It is disappointing to see how little progress has been
made in answering these questions since work on root hairs was reviewed by
Cormack (46). Some resent research on the development of root hairs has been
reviewed by Robards (159), but no clear ideas emerge about what triggers
hair-forming cells (trichoblasts) to extend their walls, or what physiological
factors determine how long extension of the hair will continue. It is evident that
the latter process is under genetic control. Species differ from one another in
predictable ways, and within species selection lines can be made that differ in
root hair length (27, 28). Root hair length in selections of Trifolium repens cv.
tamar was shown to be heritable (27) and was positively correlated with
phosphate uptake and growth from a P-deficient soil, provided that mycorrhizal
propagules had been eradicated (28). When present, VAM obscured all effects
of root hairs and plant growth improved generally. Such results discourage
further attempts to manipulate root hair length as a means of increasing the
efficiency of phosphate absorption, but it is possible for hairs to have effects on
the absorption of other nutrients, e.g. K+ (67, 108), which are probably not
passed to the host in significant amounts by V AM.
Root hair characteristics on crown roots of Oryza sativa were strongly
correlated with the meristem size and rate of elongation of the axis (107). The
length of hairs and their elongation were positively correlated with apical
growth rate of the root and perhaps to the carbohydrate status. Exogenous
cytokinin applications (kinetin) strongly stimulated root hair production and
elongation in Raphanus sativus (17) and Trianea bogotensis (2). The activity of
apical meristems can be related to the synthesis of cytokinin, its basipetal
transport, and the apical dominance of the axis, but in many other instances
where hair production and growth can be stimulated or repressed it is difficult to
see a direct role for cytokinins. Cormack (46) lists numerous factors known to
84 CLARKSON
influence root hair production, including soil aeration, carbon dioxide partial
pressure, humidity, mechanical influences of the substrate including bending
and abrasion, and calcium concentration. In addition, low concentrations of
ethylene can cause copious root hair development in water-cultured cereal
plants (178), while in Epilobium spp (71) root hair elongation is inhibited at 4
ppm ethylene in solution. It is unlikely that each of these perturbations affects
root hairs by entirely separate processes; there seems to be a clear need for
purposeful research on this matter.
ROOT HAIRS AND THE SYMPLAST Root hairs represent the most distant
outposts of the root symplast. Vakhmistrov (196, 197) and his colleagues make
the interesting suggestion that the quantitative significance of root hairs as a

pathway for nutrient intake may be reflected in the frequency of plasmodesmata
in the junction between a trichoblast and its neighbors. The intensity of
symplast fluxes across ajunction is often indicated by plasmodesmatal frequen
cy (89). In the aquatic plant Trianea bogotensis, trichoblasts had twentyfold
more plasmodesmata connecting to the underlying cortical cells than were seen
in neighboring hairless cells (196), whereas in Raphanus sativus the difference
was about twofold (197). This interesting comparison needs to be extended to
other species, and some attention should be given to the abundance of root
hairs; as it stands, this work poses interesting questions about why a water plant
should localize its nutrient absorption in root hairs and how the very high
frequencies of plasmodesmata are derived.
The absorption of phosphate (195) and other anions (116, 165, 194) may be
via a proton cotransport mechanism. In this connection it is interesting to note
that an electric current of about 2 /-La em - 2 , largely carried by H+ appears to
,
enter the tips of root hairs in barley and leaves the surface of the root beneath the
root hairs (20 I ) .
WALL STRUCTURE/PERMEABILIT Y The outer wall surface o f root hairs

appears to have the interstices of cellulose fibrils impregnated with some
material (205); earlier literature suggests that this was "cuticle" (171), but this
conclusion was based on equivocal histochemical tests. Whatever its nature, it
appears to make the walls of root hairs remarkably resistant to degradation
(160) by mixtures of powerful wall-degrading enzymes, e.g. driselase. The
extent to which the deposition influences the functional life of root hairs is
unknown; what is certain is that in diverse species, root hairs are persistent
structures. Young root hairs in wheat, 25 mm from root apex, had a hydraulic
conductivity similar to that in hairless epidermal and cortical cells (106). These
values weiedetermined using a micropressure probe (211), and clearfy this
technique could be applied to root hairs of increasing age to see if the growing
resistance of their walls to enzymic hydrolysis was paralleled by resistance to
water uptake.
Modification of Rhizosphere Nutrient A vailability

by Plant Roots
In the past much attention has been given to the modification of soil properties
by microbes in the rhizosphere (163), in this discussion I wish to emphasize that
plant roots themselves can substantially change the properties of the soil in their
vicinity and promote the release of nutrients from soil minerals . These process
es show that the actual nutrient supply to the root surface cannot be estimated
only from convection or diffusion of ions from the labile pool in the bulk soil .
ECOSEMANTICS There are large numbers of microbes in the rhizosphere

which are wholly or partly dependent on the carbon compounds that leak or are
exuded from roots. The types of materials released are those found in signifi
cant amounts in root cells, e.g. sugars , amino compounds, organic acids, and
phosphate esters . The carbon cost of this leakage will be considered again later,
but it can amount to as much as 20% of the total photosynthesis.
The dynamics of the rhizosphere and its ecology are complex (139, 163), and
its small scale causes formidable experimental difficulties. Jargon of a not very
helpful kind often proliferates when practical approaches to a problem are hard
to find-the semantics of the rhizosphere seem to have provided already a
professional niche. Descriptions of rhizo-zoogleae, polyparabioses, bioce
noses, microedaphons, and lithobionts (145) arouse in this reviewer unkindly
recollections of the "emperor and his new clothes" (Hans Christian Andersen).
POLYSACCHARIDE SECRETIONS Polysaccharides of several kinds are pro

duced at the surfaces of various cell types of roots and by microorganisms.
These materials gum soil particles together thereby improving or maintaining
porosity of the soil. Root cap cells secrete an amorphous polysaccharide slime
which serves to lubricate the root tip as it penetrates soil pores. It is chemically
distinct from mucilage of granular or fibrillar structure that is produced at the
surface of epidermal cells (200). Plant-derived mucilages seem to be relatively
labile and are more readily hydrolyzed that those produced by bacteria; this is
used as a basis for distinguishing between them in histochemical and ultra
structural stody of the rhizosphere (72). Mucilage is released from the
epidermal surface when a thin investing layer of cuticular material becomes
mechanically ruptured or chemically destroyed by soil microbes . It seems to be
derived from the primary wall layer and has a granular layer (72). It is not clear
whether this synthesis is stimulated by mechanical abrasion or microbial
factors, although it has been noted frequently that mucilage production is
greater in nonsterile than in sterile soil and that carbon losses from roots are also
greater. Fibrillar outgrowths of polysaccharide chains have been seen to project
into the soil and establish minutc bridges to the root surface (124). Both this
fibrillar material and the more extensive granular mucilage increase soil-root
contact.
86 CLARKSON
The most unusual discovery in the field was reported by Vermeer & McCully
(200), who showed that root cap cells from Zea mays, sloughed off during
passage of the tip through the soil, remain alive in the rhizosphere, presumably
taking their chance at securing substrates from the root along with all the other
inhabitants, and continue to secrete mucilage. The quantity produced was
enough to gum soil particles to form a sheath covering all but the apical 25 mm
of nodal roots. In other species it seems that the root hairs can be a source of
mucilage which gums sand particles together to form the sand sheath common
ly found around roots from arid environments (22). A more specialized sheath
develops around rice roots in anaerobic waters or muds. The diffusion of O2

[rom the root aerenchyma into the outer medium causes iron to become
oxidized and deposited as iron oxyhydroxide over the whole root surface (32).
It seems certain that these pellicles of soil , sand, or oxide must impede nutrient
and water flows to the root surface, but they may develop when plant survival is
given higher priority than mineral nutrition.
Soil aggregates (crumbs) can be stabilized by mucilages of some species ,
e.g. Lotium perenne (154, 192) and Medicago sativum (154). Organic acid
secretion from roots can, however, decrease aggregate stability possibly by the
removal of Al and Fe from organic matter (155). Extensive changes in the
micromorphology of a silt loam were observed during the growth of Phaseolus
vulgaris (167); silt particles broke down and there were increased levels of
amorphous AI , Fe, and Mn.
ACID SECRETION Some species are recognized as being particularly effective

in obtaining phosphate of P-deficient soils, e.g. Lupinus albus (74), Fagopy
rum esculentum (137), and Brassica napus (87). Each of these species acidifies
its rhizosphere by simple proton extrusion. Even when presented with N03 as -
sole N -source, B. napus cv. Emerald lowered the pH of the soil near the root
surface from 6 . 5 to 4 . 1. This pH change increased by ten times the P available
to the roots (87) and was probably unrelated to release of organic acids by soil
microorganisms which would have been within the buffer capacity of the soil
(93). The pH change was induced by P-deficiency when readily available P was
exhausted and root competition was severe. The pH change in the rhizosphere
was attributed to the excretion of H+ to compensate for cation absoption
unbalanced by anion uptake (93). This view is based simply on the quantities of
ions in the plant and is not mechanistically based. The apparent induction of
proton pumping during P-deficiency provides a most interesting opportunity
for experimental work to get a clearer understanding of the sequence of events
leading to increased H+ -ATPase activity at the plasmalemma. Fractionation of
the soil P before and after plants had grown in it showed that acid-soluble P and
residual P had been depleted in addition to the exhaustion of exchangeable P,
but there was no evidence of net hydrolysis of organic P (94) . Measurements of
K+ uptake from rhizosphere soil of B. napus (l08) suggested that the availabil
ity of K+ was also increased; K+ extracted exceeded exchangeable K+ by a
factor of 2.
An interesting technique (131) for perfusing rhizosphere soil with dilute agar
containing a pH indicator dye showed that roots of eicer arietinum (chick-pea)
also changed soil pH from 6.0 to 4.5 in the rhizosphere with either N03- or
NH4 + as N-source; this behavior was seen in Zea mays only with the latter
N-source. Rhizosphere acidification in dicot species, e.g. Helianthus annuus,
is induced when plants become iron-stressed and can be accompanied by the
release of reductant (21 , 1 62). Acid and reductant release have been described
as the most important features of proteoid roots of Lupinus albus in nutrient
acquisition (74). Particulate CaHP04 and MnOz were demonstrably solubil

ized when roots grew across agar plates containing the suspended minerals.
The authors point out that proteoid roots, with their numerous short fine
branches and profuse root hairs, do not provide a particularly effective geome
try for P-acquisition by diffusion because of intense competition between the
various adjacent surfaces, but they do provide a very effective secretory surface
for "mining" soil minerals (74, 75). Wheat intercropped with L. albus was able
to draw upon the enlarged pool of P, Mn, and Fe produced by mineralization
promoted by proteoid roots (73).
ENZYME RELEASE Nutrient deficiency, usually P-deficiency, frequently

leads to increased cellular levels of phosphatase enzymes which may leak into
the cell walls and into the surrounding mcdium where Pi may be released by
hydrolysis of phosphate esters . This role is better resolved for aquatic ( 1 6) than
for terrestrial plants, but has been shown to occur in cultures of ectomycorrhizal
fungi (25). In roots of Trifolium subterraneum there is little doubt that acid
phosphatase activity of both cell walls and extracellular solution increased as
the tissue P concentration fell (66). In Cucumis sativus calcium deficiency
promotes equally impressive increases in the activity of both acid and alkaline
phosphatases which are released into the root apoplast and the bathing solution
(209, 210). It is not yet clear whether the role of these enzymes is to release Pi
from soil organic P or to act as a trap for P-esters leaking out of the root and
rendering their Pi into a reabsorbable form .
Dracup et al (66) calculate that the hydrolytic capacity of acid phosphatase
released by T. subterraneum roots was several hundred times greater than that
needed to acquire sufficient P if limitless substrate was available to the enzyme.
It is on this last matter that the significance of phosphatase release depends; the
most abundant organic P compounds, inositol phosphates, and phytates are
poor substrates for the enzyme, and the movement of the protein through the
soil to the substrates is likely to be slow. In Brassica napus, acid phosphatase
increased fivefold in the rhizosphere soil as the plants became P-stressed (94),
88 CLARKSON
just as in T. subterraneum, but there was no evidence at all of any net

mineralization of organic P while the roots were successfully "mining" acid
soluble P by their proton release (93).
CONCLUSIONS The roots of some species are capable of modifying soil

structure directly and increasing nutrient availability by improving soil/root
contact and by chemical extraction. These activities appear to be in addition to,
but are independent of, similar changes brought about by rhizosphere mi
crobes. They would seem to be inducible when nutrients are in short supply.
We need to learn more about the physiology of this induction and the genetics
of acidification and reductant release: genotypic variation in response to iron
stress, which involves both processes, is well known (21). There may be some
scope for selection for effective "mining" of nutrients by roots in some species
and scope for development of intercropping of effective with noneffective
species.
MYCORRHIZAS
Significant Nutrient Uptake into the Host
The nutritional significance of symbioses between fungi and roots to form
various kinds of mycorrhizas is generally much more obvious in trees and in
species that grow in natural plant communities. For many woody species with
relatively coarse and unbranched roots, often lacking root hairs, there is an
obligate requirement for mycorrhizas to obtain adequate supplies of mineral
nutrients (11, 182) . For the same reasons discussed earlier for root hairs, the
exploratory geometry of the root system is much improved by the presence of
external fungal hyphae which can extend into the soil far beyond the shells of
nutrient-depleted soil that may surround the root. Therefore, it is no surprise to
find that myeorrhizae are most intensively studied with respect to phosphate
acquisition. Evidence also exists for significant contributions to zinc and
copper nutrition by the hyphae of the mycorrhizas in some species; these ions
also have low rates of diffusion in soil. There are numerous reports where
mycorrhiza formation has been correlated with general improvements in nu
trient foraging by root systems, but such improvements are often consequences
of improved phosphorus nutrition and root growth. Tracer experiments using
15N03 and 15NH4 indicate that nitrogen absorbed by hyphae can be transferred
to the host, but there was no evidence that the N-status of the host was increased
by mycorrhizas (4, 5). Water uptake is sometimes confounded with these
effects on root growth, but some reports (3, 90) have been careful to show that
mycorrhizal roots have increased water inflow rates per unit root length. Some
doubt remains, however, whether the flow of water that enters the host via the
fungal hyphae is of much consequence in the total water economy of the plant
(45).
The copper nutrition of citrus plants appears to be adversely affected by

addition of phosphorus to the soil (190); this effect seems to be correlated with
the suppression of vesicular-arbuscular mycorrhizae that occurs when plant P
status is high. The most convincing demonstrations of mycorrhiza/micronu
trient interactions have been in soils that are sufficiently rich for there to be no
mycorrhiza/phosphate nutrition interaction . In such conditions mycorrhizal
(M) leek (Allium porrum) plants infected with Glomus mosseae grew much
more rapidly than nonmycorrhizal (NM) plants and extracted much larger
amounts of copper from the soil; addition of copper to the soil progressively
diminished the difference between the M and NM plants (79). Similar un
equivocal results have been reported for zinc (44, 185). External mycelium of
Glomus Jasiculatus has been shown to translocate 35sol- into mycorrhizal

onion plants , indicating a role for V-A mycorrhizae in sulphur nutrition (157).
In this effect it seems that a further interaction with phosphate nutrition may be
the prime reason why sulphate uptake by the host was markedly increased when
phosphate stress was relieved by mycorrhizal infection (158).
Fungal Injection and Phosphate Nutrition

P-STATUS AND INFECTION The phosphorus status of the host plant is nega
tively, and its carbohydrate 'status positively, correlated with fungal infection
(92, 104). Since Pi and sugars are exchanged between host and fungus it is not
surprising to find these as factors regulating the extent of the symbiosis. Yet
there is sharp divergence of view about the interaction of these two factors on
infection of the root. Phosphorus-deficient plants may release much larger
amounts of sugar and particularly amino acid into the rhizosphere in some
circumstances. In Sorghum increased sugar leakage was negatively correlated
with the concentration of reducing sugar in the host root, although amino acid
concentration and leakage were greatest in the most severely P-deficient plants
(84). Substrate leakage has been attributed to decreased abundance of phospho
lipids in host cell membranes in P-deficient roots of Sorghum and Citrus (151).
The substrates released from the root into sand which contains only propagules
of the fungus may stimulate the germination of spores and early development of
hyphae of the fungal symbiont (84). In natural soils the outcome of substrate
additions to the rhizosphere is difficult to predict. Apparently the growth of
microorganisms, which are normally much more abundant in the rhizosphere
than the propagules of V A fungi, is likely to be stimulated, while the opportuni
ties for substrate diffusion of more than a few micrometers from the root surface
is slight. Evidently spore germination is not influenced by the presence of host
roots in soil (150, 166), nor do germ tubes and hyphae appear to grow
preferentially toward host roots . There seems to be a large element of chance in
the establishment of infection; the most influential factor is the size of the
inoculum (166).
There is unequivocal evidence that low carbohydrate status in the roots
90 CLARKSON
attached to shaded or defoliated or high nitrogen status plants significantly

reduces infection (92). Some other environmental influences that reduce root
growth, especially when leaves are strongly illuminated, increase carbohydrate
levels, but not all such conditions, e.g. low root temperature (45), stimulate
infection.
PHOSPHATE ABSORPTION BY FUNGAL H YPHAE AND M YCORRHIZAL
ROOTS Inorganic phosphate from the soil solution is absorbed by external

fungal hyphae, sometimes at considerable distances from the root surface in
both VA and ectomycorr�izas (156, 176). The transport mechanism across the
fungal plasmamembrane does not seem to have been studied . Unless it differs
from other fungi and yeasts, it is likely to be a 2 proton/Pi symport depending

on a H+ translocating ATPase to produce the required proton motive force to
drive the cotransport (12). Opportunities for studying the process are limited
because V A endophytes cannot be grown in culture, although the fungi which
form ectotrophic mycorrhizas can be. Various systems have been devised
which effect a physical separation between host roots and external mycelium in
VA mycorrhizas (45, 156, 166), and there seems to be no reason in principle
why microelectrode studies of membrane potentials and measurements of
short-term tracer influx and LlpH could not be made on these hyphae . Two
recent studies claim that mycorrhizal infection increases phosphate uptake by
roots in solution culture (54, 98) by lowering the apparent Km. In tomato,
3
short-term uptake of 2Pi by excised mycorrhizal roots (54) indicated a lower
Km (1.6 J-LM) than in nonmycorrhizal roots (Km' 3.9 J-LM) over an external
concentration range of 1-20 J-LM Pi; over the external concentration range
30-100 /-LM Pi there was no difference in Km. It is difficult to imagine that the
increased tracer absorption, which occurred at the lower concentrations, re
sulted from the very small amount of external mycelium present on roots that
had been removed from sand culture. The effect would seem to be on the
properties of the transport system of the host root. The same may have been true
in the longer-term observations on growth and net phosphate intake by mycor
rhizal Manihot esculenta (Cassava) grown in solution culture (98). Changes
in the properties of phosphate uptake by the host root tissue are likely to be of
little long-term significance in P-deficient soils where the root quickly be
comes surrounded by a shell of soil depleted of P. The Km of the external hy
phae may well be lower than in the host root, but this matter has yet to be
confirmed.
TRANSLOCATION OF Pi WITHIN HYPHAE Much of the Pi entering the hyphae

is sequestered in vacuoles where it is converted into polyphosphate (PPi) by
polyphosphate kinase. In mycorrhizal associations of different kinds these
vacuoles contain large granules which by electron-probe microanalyses have

been shown to contain very high concentrations of P relative to the remainder of
the vacuole and the cytoplasm (47, 183, 184, 203). The vacuoles containing the
granules move toward the internal hyphae, and hence the host, by cytoplasmic
streaming. In the intercellular hyphae the granules are very numerous, but they
decline in frequency in the branches of active arbuscules and are completely
absent in senescent ones (203). Cox et al (47) made a quantitative study of the P
content of granules, the volume fraction of the cytoplasm they occupied (ca
0.8 %), the rate of cytoplasmic streaming, and the number of points per unit root
length where hyphae entered the host. From these data they calculated that the
flux of granule-derived P through the entry points was 2 to 7 X 10-8 mol cm-2
s 1 This value is somewhat larger than estimates based on Pj accumulation by

-
.
mycorrhizal plants which gave values between 10-9 to 10-8 mol cm-2 s 1 and-
suggests that degradation of the PPj granules could account readily for P fluxes
into the host. The release of Pj from PPj granules is associated with alkaline
phosphatase activity in the vacuoles in the arbuscule (76) and the activity of
endo- and exo-polyphosphatase (26). The two polyphosphatase activities were
shown to be located exclusively in the arbuscules and internal hyphae (26); by
contrast, polyphosphate kinase activity was found only in external hyphae.
Thus a picture emerges of PPj synthesis in the hyphae in the soil-this would
serve to keep internal Pj concentration low and prevent repression of the
transport mechanism at the plasmalemma-followed, after translocation, by
PPj breakdown in the hyphae associated with the host. The ingenious aspect of
the work of Capaccio & Callow (26) involved partial digestion of the host root
by cellulase and pectinase which left intact arbuscules and associated hyphae
and permitted analysis of their enzymatic activities; external mycelium was cut
off prior to this digestion and its enzymes analyzed separately.
Although it seems very likely that the delivery of P to the internal hyphae
depends on cytoplasmic streaming, the one recorded attempt to disrupt the
process by cytochalasin B and examine the consequences was not very satisfac
tory (45). The external hyphae were treated for 2 days with the drug before
labeled Pj was supplied and its movement to the host recorded. Cytochalasin B
usually acts very quickly on streaming (159), and over a 2-day period hyphal
growth and metabolism are likely to have been greatly disturbed. The observed
inhibition of P-transfer to the host could, therefore, have resulted from inhibi
tion of Pj uptake from the medium. It is worthwhile being cautious on this point
since it has been shown that the inhibition of visible cytoplasmic streaming by
cytochalasin B did not significantly influence the radial transport of K+ in
barley roots, which probably occurs in the symplasm (82). Cooper & Tinker
(45) also showed that the amount of P translocated within the hyphae responded
markedly to transpiration by the host, and this suggests some mass flow-linked
component of the Pj movement.
92 CLARKSON
HOST-FUNGUS INTERACTION IN THE ARBUSCULE The relationship between

the host cells and the arbuscules of the infecting fungus has been subject to very
minute morphological and cytochemical examination. A classic early paper by
Cox & Tinker (48) showed that the presence of a developing arbuscule in the
host cell resulted in a massive (23-fold) increase in the cytoplasmic volume of
the cell. This was much greater than the threefold increase in plasmalemma
area resulting from invagination around the fine branches of the arbuscule. In
Zea mays cortical cells the surface/volume ratio changed from 0.13 to 1. 28
j.Lm2/j.Lm3 during arbuscule development (193). The concentration of mit
rochondria in the region of the arbuscule resembles the situation seen in the
cytoplasm of transfer cells (88),and the temptation to assume that the morphol
ogy of these cells is related to material transport between host and fungus is
almost irresistible-but again is unproven. It may be a response to infection and
be involved in the synthesis of copious amounts of a glycoprotein complex
which thickly invests the older parts of the arbuscules seen in onion/Glomus
mosseae and Ornithogalum/G. fasiculatus mycorrhizas,reported by Bonfante
Fasolo et al (19). This material is much thinner over the finer, more recently
formed, branches of the arbuscule, but when arbuscule growth ceases and
senescence begins the whole structure quickly becomes invested in the gly
coprotein complex. This process may represent some kind of "containment"
reaction by the host to infection. There is no indication that the plas
mamembrane of the host is grossly damaged or altered where it is associated
closely with that of the fungus in the arbuscule (77). The impression that it is in
the finer branches of the arbuscule, which were found to occupy 25% of the
host cell volume in Zea mays/Glomus fasiculatus (193), that the principal
nutrient exchanges between host and fungus occur, is strengthened by histo
chemical tests which indicate intense diethylstilbestrol(DES)-sensitive ATPase
activity along the host plasmalemma (135) and ATPase activity in the fungal
plasmalemma (77).
Most of these observations are compatible with the very perceptive sugges
tions made by Woolhouse (208) about the nature of the exchanges between host
and fungus. The use of the word "exchange" might be taken as suggesting some
mechanistic linkage between the movements of Pi and sugar. This speculation
does, however, outstrip the facts. The substances do not move across a single
membrane but across a pair of membranes separated by a matrix which can be
seen to contain occasional membrane-bounded vesicles (76) and fibrils of
glycoprotein. The nature of the smaller molecules and the pH in this matrix is of
great interest but is presently unknown.
The presence of the DES-sensitive ATPase in the host plasmamembrane
(135) is the justification for putting a proton pump on the host side of the space
in Figure 2. This would acidify the intermembrane space and provide the dpH
to drive sugar into the fungus via a H+ cotransport system. The same dpH and
diJ., H+ provide the driving force for H+ /Pi cotransport into the host. The
missing piece is the one which would explain why Pi leaks or is pumped from
the hyphae into the intermembrane matrix. Clearly the properties of the fungal
plasmalemma in the internal hyphae must be very different from those in the
external ones where it is likely that Pi uptake not release would be driven by
conditions such as might be expected in the matrix solution. The question is
bound to arise whether the sugar and Pi fluxes across the fungal plas
mamembrane are coupled in some kind of antiport system (191a) similar to that
in the phosphate translocator of the chloroplast envelope (95). One way to test
this idea might be to examine the effect of feeding external hyphae with glucose
on the transfer of Pi from fungus to host. If sugar enters the hyphae in response
to a metabolic demand ( = sink) of the extending hyphal tip, then, in a linked
system, Pi transfer should vary with that demand. Within the hyphae there is
likely to be a gradient of carbohydrate and amino-N which runs downhill
AlP .. PPjase
®vac
". I
ADP + Pi
Host Matrix zone Fungus

pl. pI.
Figure 2 Suggested mechanisms for the transport of Pj and sugars between fungus and host in a
fine arbuscular branch in a VAM. The primary active transport in both plasmalemmas is envisaged
as an H+ -translocating ATPase (77, 135). Passive flows of Pi and sugar into the matrix are then
driven across the opposite plasma membrane by coupling to the proton gradient. In the fungus
[P;]cyt in arbuscule branches may be high because of breakdown of PPj contained in vacuoles; these
are conveyed to the arbuscule by cytoplasmic streaming (stippled arrow). Pi uptake by the host is
envisaged as a 2H+ /Pi symport (195). There is precedence for H+ -cotransport of hexose sugars in
fungal hyphae (176a), but this has not been worked out in VAM (91).
94 CLARKSON
toward the tips of the external hyphae. Is this gradient related to the polarization
of the hyphae with respect to its phosphatase and PPj kinase activities? Reversal
by feeding hyphal tips directly with substrates might provide an insight into a
number of questions of this kind.
Manipulation of Host-Fungus Association

The zest with which these intriguing questions are being pursued seems to
contrast with a reduction in optimism about manipulating host/fungus interac
tions of crop plants by "mycorrhizal engineering . " Tinker (191) takes a very
sanguine view of improvements of the effectiveness of the associations . While

it is very clear that isolates of various species of fungus can vary in their
tolerance to various conditions and that some strains improve the yield of a
given host more than others in phosphorus-deficient soils (1, 104, 105), Tinker
(191) concludes that "No evidence has appeared so far indicating that new
strains with remarkable yield-enhancing properties are likely to be discovered,
and the present situation continues to emphasise the severe disadvantages of
being solely dependent upon prospecting (my italics) for new material , with no
possibility of using sexual recombination as a source of variation . " The fungi
forming V AM cannot be grown in pure culture and have never been seen to
reproduce sexually. In this respect they contrast with the basidiomycetes which
form the ectotrophic mycorrhizas of woody species; with these associations the
potential for selection and improvement are greater.
REGULATION OF NUTRIENT INTAKE
The properties of ion absorption systems reflect the nutritional environment in

which roots of terrestrial species have evolved and the demand for mineral
nutrients created by growth . Natural soils usually contain the major plant
nutrients in dilute solutions ( 1 0 - 6 to 1 0 - 3 M) from which high affinity trans
port systems (System I) can extract them effectively. Flowing solution cultures
(4 1 ) and nutrient addition techniques (100) have shown that maximum growth
rate , set by factors such as light intensity and temperature, can be sustained if
plants are provided with dilute concentrations of nutrients at around the Km
values for system I absorption. This is true for both wild plants and rapidly
growing crop species . Simple calculations of daily intake of major nutrients to
maintain steady tissue concentrations at a given rate of growth show that the
necessary absorption rates are less than measured values of the Vmax' It is clear
that Vmax System I values change with growth rate in seedlings (204) and such
factors as the shootroot ratio, which influence the intensity of the demand
placed on the root system.
Although nutrient influx continues above the concentrations that saturate the
Vmax System I, the nutrient intake is not necessary for growth and, unless it is
matched by equivalent efflux, causes luxury accumulation . This may be useful

in storage of nutrients (29) whose abundance may change markedly during a
growing season, e.g. N03 - .
Short-term Modulation Related to Internal Concentration
Some apparently conflicting reports on the effects of internal nutrient status on

System I carriers for K + , H2 P04 - , CI- and sol- suggest that there are
short-term modulations of their activities and longer-term changes in carrier
numbers . Short-term modulations can be measured when cytoplasmic concen
trations of ions are rapidly altered , usually by short periods of heavy loading,
e. g. K + (80) or Cl - (164). Such experiments show, in the case of K + in barley
roots , a close correlation between [K+lroot and the Km and Vmax of the system.
Although no actual measurements were made of [K +lcyt> the results have led to
a much discussed proposal that the carrier for K+ is regulated allosterically by
cytoplasmic K+ (80, 81, 172). These short-term changes in carrier activity can
occur in the presence of various inhibitors of protein synthesis; this is taken to
indicate that carrier synthesis is not involved in the changes.
We need not discuss here the validity of ideas about allosteric regulation in
roots , but it is relevant to ask whether, in nature , cytoplasmic concentrations of
nutrients change rapidly in the way contrived in the laboratory. One purpose of
the vacuole may be to prevent this sort of thing (37). Evidence from a variety of
sources suggcsts that the cytoplasm is well buffered against changes in the
concentrations of nutrients . The use of 3 1 P-NMR on apical sections of pea roots
that had been grown for varying lengths of time in P-deficient medium showed
that over a threefold range in [Piltotal the [Pileyt was unchanged while the
[Pilvacuole varied exactly as the total Pi (120). In yeasts , release or sequestration
of ions and solutes in vacuoles buffered the cytoplasm against fluctuations in
K + , Mg2 + Pi (126), and amino acids (99). In a recent model of K+ compart
mentation in higher plant cells, Leigh & Wyn Jones ( 1 23) assume that cytoplas
mic K+ remains constant at about 150 mM while vacuolar concentration may
vary over a fivefold range. At a critical low concentration in the vacuole,
around 20 mM , [K+lcyt cannot be sustained and protein metabolism and growth
are disturbed.
Longer-term Adjustment of Carrier Activity
Even if cytoplasmic ion concentrations are relatively stable, it is evident that

the kinetic properties of carrier systems can be strongly influenced by the
steady state nutrient supply to which they are exposed. The greater numbers of
more avid carriers found in plants that are mildly nutrient stressed are likely to
involve increased carrier synthesis. In Hordeum vulgare the Vmax of System I
H2P04 - and sol- transport increased during stress-induced demand, but
96 CLARKSON
there was no change in Km ( 1 1 8 ) . In the same species, K+ stress induced first a

marked fall in Km (from 53 to 1 1 flM) , followed 3 days later by a twofold
increase in Vmax (70) . Lee ( 1 1 8) has pointed out that the practical effect of
changes in either Vmax or Km is to increase the rate of uptake from very dilute
solutions; thus they represent the plant's early response to maintaining nutrient
inflows in response to diminishing supplies of nutrients. These changes are
usually initiated before growth rate has been affected by nutrient deficiency
(38a, 42, 69) .
In a variety of circumstances, steady-state concentrations of nutrients in
roots and shoots seem to be independent of external ion concentration ( 1 3 , 4 1 ,

1 25) and environmental variables such as temperature ( 1 73). As indicated
above, this homeostasis can be achieved by adjustments to carrier activity and

also by modifying growth rate and pattern (see below). It has been observed,
however, that steady state concentrations of ions in roots (largely in their
vacuoles) is maintained so as to be as close as possible to a "set" value. Much of
this work derives from the rather puzzling influences that Cl - and N03 - have
on one another's absorption. Interpretation of results is made complex for
several reasons: first, that the accumulation of a given anion, e . g . N03 , -
responds to the "set" value for [N03 - + Cl - ] rather than to [N03 -] alone (at
least it does so in roots oflow N03 - status); second, the principal control points
seem to be the anion fluxes across the tonoplast rather than the plasmalemma.
Cram, in a series of papers (49-5 1 ) , and Smith ( 1 77) suggest that control of
accumulation is exercised by some unspecified feedback signal , possibly
cytoplasmic pH, generated by any departure from the in built "set" concentra
tion; thus the tonoplast fluxes are governed by a measure of "error" or perturba
tion of the conditions in the vacuole. The fluxes at the plasmalemmma appear to
be relatively unimportant in determining the steady state [N03 - + Cl-] in
carrot storage root slices or maize roots (49, 5 1 ) . It is worth mentioning here
that more results are available for the Cl- fluxes than for those of N03 - for
obvious technical reasons. However, it has also been shown that S042 -
accumulation in carrot root is determined by regulation of tonoplast fluxes (52,
53, 1 89).
The evidence points to separate controls over accumulation of ions (=
concentration) in vacuole and cytoplasm-an arrangement quite consistent
with the separate functions of these compartments. The cytoplasm of a root
cell , in addition to managing its own affairs, is a staging post for symplast
export and assimilation of ions. Clearly it would be unsatisfactory if influx of,
say N03 - at the plasmalemma were heavily repressed because the vacuole
,
was at its "set" level of [N03 - + Cl- J (see Cram (50). After all , the growing
cells in the shoot depend on this flux for their N. It is well that roots do not go to
sleep when they are adequately supplied with nutrients.
Regulation by Efflux Control

The cytoplasmic activity of calcium ions is believed to be in the range of
10--1000 nM in higher plant cells as it appears to be in mammalian cells and
giant algae . Most cytoplasmic calcium is either bound or sequestered, possibly
in the ER (130, 1 80). The total calcium content of root cells, even if it were all
present as free ions, is far below the level predicted from thermodynamic
consideration (96, 1 28), and it seems very likely that net intake of Ca2 + is
regulated by the active extrusion of Ca2+ from the cell via a Ca2 + transporting
ATPase (212).
Nitrate moves out of cells much more rapidly than other ions, and net N03-
uptake is usually the balance between influx and efflux , both of which are
substantial and probably regulated independently (103, 1 29). Early attempts by

Jackson et al ( 1 03) to measure variations in influx made use of 1 5N-Iabeled
N03 - for which analytical techniques are relatively insensitive . Measurements
of influx were inferred from experiments lasting 0. 5-6 h in intact wheat
seedlings, from which the authors concluded that there were substantial
changes in influx with changing nitrogen status of plants . Deane-Drummond &
Glass (60) point out that during these rather extended periods of time, efflux of
15N03 - from the cytoplasm would have been substantial and that the authors
were, in fact, measuring net uptake with their tracer, rather than influx. Using
3
measurements of short-term 6CI03 - uptake by roots [as a tracer (59) for
N03 -] and continuous monitoring by N03 - selective electrodes in the external
solution , it was found that when barley seedlings were transferred from a
medium containing 10 fLM N03 - , in which the plants were N-deficient, into
one containing 100 fLM N03 - , there was initially a high rate of net N03 -
intake which declined rapidly . After 20 min the rate was similar to the rate in
"high" N plants although intitially the rate in "low" N plants was more than ten
times faster. During this great fall in net uptake, the N03 - influx as measured
3
by 6CI03 - did not change and the efflux must have risen; after an hour the
efflux was 50-85% of the influx. In these experiments it seems that net intake is
controlled by efflux rather than by regulating influx at the plasmalemma. A
similar conclusion was reached from experiments on 1 5N03 - uptake and
exchange in Phaseolus vulgaris (20). An alternative approach ( 1 1 9) to N03 -
3
uptake kinetics made use of the short-lived isotope 1 N (t Y2 = 10 min) . In
barley it was found that influx in roots did vary with N status . Vmax for System I
N03 - transport increased significantly from 3.9 to 5.7 fLmol h - 1 g - l fresh wt
as the tissue N03 - was depleted from 81 to 3 fLmol g - l fresh wt by N03-
deprivation over 3 days; there was no change in Km (119). This change in Vmax
is very smaJl compared with what can be found for other ions; for example for
sol- in Macroptilium atropurpureum, Vmax is increased more than eightfold
after 2 days of S04- deprivation (39). This confirms the view that the wide
98 CLARKSON
fluctuations observed in net N03 - intake are unlikely to result from changed
influx (60). In Chara it has been shown that N03 - efflux is sensitive to
metabolic blockade and can be greatly increased in the presence of NH4 + in the
external medium (58); N03 - efflux increased when NH4 + was fed to barley
(6 1 ) , Arabidopsis thaliana (65), and wheat ( 1 38) .
Efflux of Pi from the aquatic plant Spirodella varied with the P-status and
growth rate of the fronds ( 1 5). Where plants grew exponentially at 25°C, efflux
was 8% of the influx from 1 mM Pj, but this decreased to >2% when plants
"
were mildly P-stressed. A rapid reduction in growth rate achieved by reducing
the temperature from 1 5° to 5°C greatly increased the efflux even as the influx
declined. In this species net uptake of Pi seems to depend on regulation of both
fluxes (15); this has also been suggested in other species ( 1 36).
Fluxes Through the Symplast

Experiments with divided root systems strongly suggest that carrier levels or
affinities for K+ (69) , H2P04 - (42 , 68 , 69) , and sOi- (39) can be augmented
in roots which are themselves receiving an adequate nutrient supply and which
contain relatively high nutrient concentrations . Inflows into such roots can be
increased if other parts of the root system are deprived of the nutrients in
question. The plasmalemma flux responds, therefore, to remotely located
demand. With phosphate in particular, nearly all of the augmented flux is
channeled toward the xylem (38, 38a, 69) . These results point to some rela
tionship between the rate of release of ions into the xylem and the plasmalemma
influx (39, 69, 149). It is possible that the symplast is a separate compartment
within the cytoplasm, the ER for instance, which can establish a high priority
for ions entering the cytoplasm across plasmalemma and tonoplast. The cytosol
concentration could be lowered if the symplast flux to the xylem was large
relative to these imputs (39, 69) . Suggestions of this kind to explain cytoplas
mic K + compartmentation in barley roots have been advanced before (8, 97) .
There is now evidence that there are electrogenic ion transporting mechanisms
in the stele of roots (62, 1 43) and that these may be involved in regulating the
ion release into the xylem (40) . If these mechanisms can be induced to release
ions more rapidly , by nutrient stress or demand, depletion of the cytoplasm by
the symplast flux could be possible. The augmentation of plasmalemma
absorption capacity might be expected to follow from this if the release of ions
from the root vacuoles was slow by comparison.
The Size of the Absorbing Surface

When some nutrients limit plant growth, notably N and P, the roots become
relatively stronger sinks for carbohydrates than shoots. This shows itself in an
earlier reduction in shoot growth during stress than in root growth [e . g . in
Plantago spp. ( 1 09, 1 1 0)] . An explanation is that roots, being nearer the
nutrient supply , comer limited inflows for their own purposes and experience
less stress . Although this response is very common in crop plants , which all
belong to the plant categories described as "competitors" or "ruderals" (85,
86), it is not found or is far less marked in many slow growing "stress
tolerators" (33). The mineral nutrition of this latter group of plants has received
little consideration. Chapin et al (31) compared a P-strcss tolerant alpine grass
Chionochloa crassiuscula with another species C. pallens which inhabits soils
of greater P-status and found that the stress tolerator, in addition to showing less
flexibility in the shoot:root ratio, lacked the fine control of nutrient intake seen
in the more ruderal type of species. Although the growth of stress tolerators is
unresponsive to high nutrient supply, they appear not to repress ion uptake
mechanisms when confronted with surplus nutrients and often have higher
nutrient concentrations in their tissues than crop plants (30, 3 1).
Plants growing in soil often show much greater flexibility in shoot root ratio
than those grown in laboratory solution cultures. In laboratory conditions the
shoot root dry weight ratio of barley fell from 2.9 in high P plants to 1 . 4 in
P-deficient plants. In these experiments P-stress was abruptly applied by
leaving P out of the culture solution . In soil, continuous subsufficient levels of
P seem to produce much larger roots in wheat. On a P-deficient sandy loam the
shoot root ratio was 0.26, whereas in the same soil + P fertilizer the ratio was
1 .33 in 3-week-old plants ( 10).
The relative expansion of root surface will have the effect of reducing the
flux necessary to sustain a given nutrient; it can also reduce the minimum
concentration necessary to maintain the inflow (see 204). This effect is seen
during the development of seedlings into young plants-a phase in ontogeny in
which the root surface per unit shoot weight increases (204, 207).
Conclusions
The maintenance of appropriate cellular concentrations of nutrients appears to
be the purpose of the regulation of carrier activity and control of efflux
described above. Roots absorbing a relatively immobile nutrient from a dilute
unstirred soil solution inevitably reduce the concentration at the root surface to
a low level. Increases in Vmax' even in the absence of a change in Km , can assist
in scavenging the dilute solution for ions because, in such circumstances , the
Michaelis-Menten equation simplifies to
where Clo is the concentration at the root surface. Eventually the concentration
will fall to a point where influx is negligible in comparison with demand.
1 00 CLARKSON
Modulation of the kinetics is, therefore, an early response to nutrient stress and
occurs before changes in growth rate can be measured (38a, 39, 42 , 65 , 70,
1 22).
The second response to limiting supplies of N and P , possibly for S and K
also, is the inhibition of overall growth and the relative enlargement of the root
system. This is often accompanied by a fall in Vmax as demand on the root
system lessens (39) . This morphological adjustment also has limits . Beyond
this point the ability of the plant to remain healthy while the overall growth rate
is progressively reduced is the only practical approach to regulating nutrient
intake-a regulation imposed from outside the plant.

THE ENERGY COST OF MINERAL NUTRITION
Many who work in agricultural research find themselves hag-ridden by frisky

cost-benefit analysts , so to have some answers prepared to the question-"what
does mineral nutrition cost the plantT-might be handy. One should first
inquire whether broad sense or narrow sense costs are being discussed. In the
broad sense, costing should include respiration to support the growth and
maintenance of the root system, the energy content of the carbon substrates lost
directly to the rhizosphere by exudation and leakage, and the cost of direct
substrate transfers to mycorrhizal fungi. In the narrow sense, the cost would be
the fraction of maintenance respiration which is expended directly on the
activity of ion uptake processes , on nutrient movement in the symplast and
release into the xylem. It is much easier to find published estimates for broad
sense than for narrow sense costs.
Broad Sense Costs
ROOT GROWTH AND MAINTENANCE The cost of growing the root system
might be estimated from theoretical considerations of the ATP and NADH
requirements for biosyntheses ( 1 1 1 , 147) or by extrapolation from measure
ments of oxygen uptake by growing plants ( 1 1 4) . The former method predicts
the energy needed to synthesize a unit of biomass of a given composition. The
cost varies with the type of biomass produced, e.g. a high protein content
implies a greater cost than a high polysaccharide content ( 147) . The amount of
oxygen consumed in respiration can also be estimated if the p:o ratio is known .
The total respiration of an organ is of course greater than the growth respiration
associated with the synthesis of biomass. In all cells the turnover of enzymes,
structural components such as membranes , and the compartmentation of ions
and substrates against gradients of free energy contribute to the "maintenance"
respiration. These costs too have been subjected to theoretical analysis by
Penning de Vries ( 146) , who estimated costs of 7-1 3 mg glucose d- 1 g- l dry
wt for protein turnover and 6-10 mg glucose d - I g - I dry wt for compartmenta

tion of ions and substrates in leaves. These estimates fall in the lower part of the
range of values derived from experiments of various kinds. No estimates were
made for roots , but one might predict that protein turnover in them would be
less costly (they have no Rubisco and usually much less NR-the major
contributors in leaves because of their quantity and rapid turnover respectively)
and ion transport costs would be greater. A method derived from partitioning
respiration in micro organisms ( 1 48) allows estimates of "growth" and "mainte
nance" respiration from plots of oxygen uptake/dry weight gain against root dry
weight for plants in a linear phase of growth ( 1 14). The maintenance respiration
(intercept with the y axis) and growth respiration (slope of the lines) differed
greatly between roots of different species ( 1 12). Oxygen consumed per unit
root growth was invariably much greater than values predicted from theoretical
considerations where the P:O ratio of 3 was assumed ( 147) . It is hard to convert
the units used by Lambers ( 1 12), mg02 h 1 g I dry wt, into milligrams of
- -
glucose because of uncertainty about the P:O ratio, which in roots is evidently
less than 3 because of the flow of electrons along the alternate , cyanide
resistant pathway [see Lambers ( 1 13) and Laties ( 1 17) for rather different
views about the significance of this] . Lambers (115 , 133) points out that
conversion efficiency of substrates is low in roots because of the activity of the
alternative pathway, and both growth and maintenance respiration have a
wasteful component-a problem made more acute by rapid changes in electron
flows along the alternative pathway as circumstances change. In general,
however, the conversion efficiency of substrate into ATP is appreciably lower
in roots than in leaves ( 1 1 2 , 1 86, 1 87) .
A number of enviromental factors can influence the relative size of the root
system, one of which, nutrient supply, has been mentioned earlier. Increased
size of the root system relative to leaf area in the face of nitrogen or phosphorus
deficiency must increase the "cost" of the root system in the broad sense, but
costs may not increase directly in proportion to size. In some populations of
Plantago lanceolata, which increase their root growth rate relative to that of
shoots in dilute nutrient solution, there appears to be a very marked increase in
conversion efficiency in comparison with slower growing roots at a high level
of nutrient supply (110) . Conversely, a population of P. major, which has l ittle
ability to vary its root growth relative to shoot growth, does not decrease its
oxygen uptake when transferred from concentrated to dilute nutrient solution
(109) , as has been seen in P. lanceolata. Lambers ( 1 1 2) found that the roots of
mature plants of Senecio viscosus growing in dilute solutions had about half
the growth respiration rate found in roots growing in "normal" nutrient solu
tion; they also had a relatively large root system (shoot root 2.5 as opposed
to 4.5). Lambers (112) concluded that plants with a high shootroot ratio
have a low conversion efficiency; in other words , they make profligate use
1 02 CLARKSON
of substrate supply which greatly exceeds requirements for growth and main
tenance.
One is left with the impression that supply of substrate is unlikely to be a
limiting factor for growth or nutrient transport in well-illuminated plants , and
that when an increase in root size occurs which will improve nutrient "forag
ing," the increased carbon cost is offset partly by increased efficiency of
substrate conversion.
ROOT EXUDATION There is no doubt that many carbon compounds are lost
from roots by exudation or leakage into the rhizosphere . Numerous estimates of

the intensity of this process range from 2% of the carbon fixed by the plant to
values greater than 20% ( 163 , 206) . This is an area where quantitation is
fraught with problems. The simplest approach is to grow roots in sterile media
and measure what comes out. This has been done by growing shoots with a
continuous supply of 1 4COz and separating them from roots contained in
another compartment (9, 1 32, 1 3 3 , 202). In such studies the carbon lost to the
sterile soil in the form of water-soluble and insoluble exudates ranged from 5 to
10% of the carbon fixed per day. In sterile barley plants which were growing
without obvious environmental stress , CO2 evolved by root respiration
accounted for three times the amount of carbon lost by exudation . However,
limitation of root growth by water stress shifted this balance so that more
carbon was exuded or lost in sloughed-off cells than was used in growth and
maintenance respiration ( 1 34, 202). In nonsterile conditions, some experi
ments (9) showed that plants increased exudate losses from 1 2% to 1 8 % of the
carbon fixed.
Root exudation represents a continuous and appreciable drain on the re
sources of the plant. The actual amount of carbon lost almost certainly varies
with the health of the plant and its rate of growth, its nutrient and water status ,
and the types o f microorganisms i n the rhizosphere. The amount can be
equivalent to or greater than the carbon used in root respiration, so we must
conclude that, in many circumstances, it costs more than ion uptake processes
(which represent about 20% of the maintenance respiration). It is difficult to
believe that this represents a sound investment for the plant, particularly if
benefit is measured simply in terms of increased nutrient availability in the
rhizosphere resulting from microbial activity. Nrfixation in the rhizosphere of
tropical grasses (64) may be an exception. Plants frequently grow as well or
better in sterilized soils than they do in the presence of microbial associates if
the phosphate supply is adequate .
MYCORRHIZAS With a few exceptions , all plant families develop symbiotic

associations with fungi to form mycorrhizas. Carbon balance and respiration
measurements indicate that mycorrhizas are stronger sinks for fixed carbon
MINERAL NUTRIENT ACQUISITION 1 03
than uninfected roots. The proportion of total photosynthesis transported to the

root system is greater in both VAM and ectomycorrhizas. There is usually more
fungal biomass in the latter type , hence the carbon utilization is likely to be
higher (9 1 ) . The fungal sheath in Fagus mycorrhizas accounted for 50% of the
O2 uptake and CO2 output while being only 40% of the weight. There is
evidence that the alternative , cyanide-resistant pathway is very active in Fagus
(43) and Salix (6) mycorrhizas. In seedlings of Pinus taeda the proportion of
fixed carbon respired by mycorrhizas was greater by factors of 1 .4 to fourfold
than in non mycorrhizal roots over a l O-month period ( 1 52) .
The carbon cost of establishing VAM associations can often be seen as a

depression of the growth of young seedlings , especially if they are adequately
supplied with nutrients . Calculations of the carbohydrate demand in the synthe

sis of fungal biomass suggest that more than 10% of that used by the root is to be
expected (9 1 ) . This is borne out by experiment. Pang & Paul ( 1 44) and
Snellgrove et al ( 1 79) found mycorrhizal roots of Viciafaba and Allium porrum
respectively to be stronger sinks for photosynthate than nonmycorrhizal roots .
In nonmycorrhizal plants, 37% (V. faba) and 30% (A . porrum) of the total
carbon fixed in photosynthesis was translocated to roots; in mycorrhizas the
proportions were 48% and 37% for the two species respectively. Most of the
extra carbon was recovered as CO2 output from the rooUsoil systems. Within
the roots the presence of the fungus increased carhon consumption in respira
tion by 74% (V. faba) and 1 8 % (A . porrum) .
The costs of maintaining the association is appreciable , probably represent
ing 5 to 10% of the total photosynthesis for V AM plants and perhaps more for
ectotrophic mycorrhizas. These costs are of the same order or larger than
estimated costs of nutrient uptake per se.
Narrow Sense Costs

It is surprising to see how little thought has been given in recent years to the real
energy costs of ion transport; uncertainty about the actual mechanisms is
probably the explanation .
THERMODYNAMIC ACCOUNTING If the electrochemical potentials of ion

species in the cytoplasm and the surroundings are known, the free energy
change involved in the uptake of each can be calculated . The energy inputs for
uphill transport can be converted into a quantity of ATP based on the free
energy released during hydrolysis. In such thermodynamic calculations there is
no consideration of the actual mechanisms coupling ATP hydrolysis to ion
transport; the cost of transport will , therefore, be the minimum possible. It is
difficult to make the necessary calculations for ion uptake by mature root tissue
because there is uncertainty about the activity of many of the ions in the
cytoplasm, especially for those which enter most steeply uphill. This task is
104 CLARKSON
simpler with Cl- ; Sanders ( 1 65) calculated that for plasmalemma chloride
influx in a variety of cells, ranging from Scenedesmus to barley roots , the
percentage of total power generated by photosynthesis and/or respiration used
to drive observed influxes ranged from 0 .03% to 6% . Only recently has
compartmental analysis been applied to N03 - (59), H2P04 - ( 1 2 1 ) , and sol
(52 , 5 3 , 1 89) in attempts to measure cytoplasmic ion concentrations. The
interpretation of the kinetics is complicated by metabolization of the ions.
If the cytoplasmic concentration and membrane potential remain constant,
the free energy gradient acting on ions will vary with external concentration;
the uphill gradient, and hence the minimum energy input to accomplish
transport, will increase for anions as external solutions are diluted. On this
basis it was calculated (35) that N03 - uptake by Lolium perenne changed from
"costing" 28 kJ mol - I in 1 . 5 !-LM N03- to 9 kJ mol - I in 1 5 mM N03 - ,
equivalent to 4 mol ATP and 1 . 3 mol ATP per mol N03 - respectively . It is
difficult to envisage a mechanism in which the hydrolysis of ATP could be
coupled to variable numbers of N03 - ions, especially since the hydrolysis
energy of ATP is rarely, if ever, wholly consumed in the reactions it energizes .
A mechanistic approach to the problem moves us nearer to the real ATP
requirement.
MECHANISTIC ACCOUNTING In the absence of knowledge of the mecha

nisms involved in ion transport, Penning de Vries et al ( 147) assumed that
active transport cost 0 . 3 mol ATP per mol ion. In microorganisms, "uphill"
transport of a number of substrates and ions by high affinity systems is
obligately coupled with the movement of protons into the cell. These cotrans
port systems probably exist in higher plants . Evidence of proton cotransports of
N03 - ( 1 94), H 2P04 - ( 1 95) , and sol- ( 1 1 6) have been found in Lemna with
probable stoichiometries of 2H+ for N03 - and H2P04 - and 3H+ for S042 - .
The maintenance of cytoplasmic pH at around 7 . 5 makes it essential that H +
entering with the anions is discharged across the plasmalemma, probably by a
H+ -translocating ATPase. The stoichiometry of this proton pump in higher
plants is not known ( 1 8 1 ) , but on the basis of what is known in Neurospora it is
likely to be 1 H + :ATP. The pump is electrogenic, giving rise to a membrane
potential sufficient to drive the divalent cation fluxes and the fluxes of monova
lent cations from all but the most dilute solutions . There may be other ATP
costs associated with a Ca2 + -efflux pump ( 1 30) and a neutral exchange of Na +
for K+ via an ATPase. Both of these costs will be small relative to the proton
pump. With the infonnation above we can simply calculate the minimum costs
of ion uptake from a solution that contains more than 1 .0 mM K + and no N a + .
Thus 2ATP per N03 - or H 2P04 - , 3ATP per S042 - are used in uptake and 1
ATP per Ca2 + discharged from the cell. Let us assume N03 - is being absorbed
at 50 !-Lmol h - 1 g - l dry weight by roots and H2P04 - and SO/- at one tenth of
2
that rate and that cytosol Ca + regulation requires 5 fJ.mol h I g - I to be
-
pumped out of the cell . The ATP required for these processes is 1 30 fJ.mol h- I
g - I . Assuming P:O ratios of 3, 2, and 1 , the processes should consume 43 , 65 ,
or 1 30 fJ.mol O2 or 0.68, 1 .04, 2 .08 mg O2 h- I g- I dry weight. These compare
with estimates of maintenance respiration for roots of 3 - 1 3 mg02 h - I g- I dry
weight ( 1 1 2) and seem quite reasonable, not being far removed from Penning
de Vries's ( 146) assumption that transport costs amount to 20% of maintenance
respiration.
In the above method ATP consumption is determined by the flux; if this
remains the same as the solution is diluted, the energy cost is unchanged. With
changing rates of nutrient supply, carrier properties or numbers (i.e. Km or

Vmax) may become adjusted to produce a relatively constant nutrient inflow .
Apart from the maintenance of larger numbers of carriers, the absorption of
nutrients need cost no more from dilute solutions than from more concentrated
ones .
RESPIRATORY ACCOUNTING The respiration of roots, especially if they are

low salt status, can increase markedly in some species when they are chal
lenged by moderate concentrations of salt ( 1 27). The magnitude of "salt
respiration" can be strongly dependent on the species of anion present and its
rate of uptake , but not on the cation. The use of this phenomenon to calculate
the energy cost of anion transport is questionable from a number of points of
view. It is not found in all species, e.g. Zea mays ( 1 70), following a salt
challenge even though anions are absorbed, and it may persist for at least 8 h
after the external salt challenge has been withdrawn ( 1 8) . It seems more likely
to reflect the rise in maintenance respiration associated with compartmentation
and salt efflux processes ( 170) . Also, the P:O ratio can change markedly when
either the salt burden or the nitrogen source is altered (63). The interpretation of
O2 uptake in relation to ion transport seems far from straightforward .
Attempts have been made to infer nutrient transport costs indirectly by
measuring respiration, growth, volume, and ion uptake in circumstances where
ion or substrate supply is perturbed ( 1 98 , 199). Variation in the four measured
parameters was obtained by root pruning and shading treatments . Growth,
maintenance, and ion uptake components of respiration were then obtained by
multiple regression analysis. Some unusually large estimates for the ATP
requirement for N03 - transport are obtained if P:O ratio is assumed to be 3. In
his calculations, Veen ( 1 98 , 1 99) appears to have ignored the contribution of
the alternative pathways to the observed O2 uptake and not to have considered
that conversion efficiency may have varied in his root pruning experiments as
the shootroot ratio changed. Recalculation of Veen' s ( 1 98) results on the basis
of a P:O of 2, i . e . allowing for 33% alternative pathway respiration, gave a
value of approximately 4 ATP per mol N03 - absorbed ( 1 1 5 ) .
106 CLARKSON
HIDDEN COSTS The narrow sense accounting should consider what costs are
involved in the turnover of carrier molecules on the transport pathway, move
ment through the symplast, and release into the xylem. With respect to turnover
there seems little to go on. One report ( 1 88) suggests that the hexose carrier in
Chlorella plasmalemma turns over very rapidly 4. 1 d- I , which makes it about
as labile as nitrate reductase. Experiments making use of amino acid analogs to
synthesize ineffective proteins ( 1 68) suggest that turnover of some crucial
protein on the transport path for 36Cl - is appreciably faster than the plas
mamembrane carrier. Movement of ions in the symplast is usually envisaged as
diffusion assisted by cytoplasmic streaming; the energy costs of the latter are
unknown . Several lines of research suggest that there are energy-consuming
transport mechanisms in the stelar parenchyma which may regulate the release
of ions into the xylem (40, 62, 143). In onion roots there appears to be proton
release into the xylem vessel which can be stimulated by fusicoccin; the activity
of this mechanism, probably an ATPase, can vary from approximately 0 . 4
/-Lmol h - 1 g - 1 fresh w t t o 4 /-Lmol h 1 g 1 fresh w t (36). Assuming a
- -
stoichiometry of 1 H + : ATP, a P:O ratio of 3, and a fresh wtdry wt ratio of 10,

oxygen consumpti on b y this mechanism would b e between 0 . 02 and 0 . 20 mg
O2 h - I g 1 dry weight. These values are smaller than those calculated earlier
-
for nutrient uptake but may not be entirely negligible .
Conclusions
If the root is seen as a system foraging for nutrients , the foregoing discussion
suggests that the energy costs of seeking out the nutrients by morphological
adjustments to the root itself, or through the maintenance of mycorrhizal
associations, or by leakage of substrates , are greater than the costs of transport
once the sources of nutrient have been reached.
CONCLUDING REMARKS
This review attempts to show that tifficient nutrient acquisition by a species

depends on numerous properties of its root system. Undue emphasis on the
characteristics of its ion uptake mechanisms and their operation in ideal
conditions may deflect attention from other salient features , such as the way its
morphology can be modified by the medium in which it grows and the demands
placed upon it. The development of the root system, its losses of substances , its
secretion of acid and ligands to the rhizosphere, and the support of its almost
ubiquitous fungal symbionts are all much greater charges on the carbon re
sources of the plant than is ion uptake, and all of them greatly influence the
outcome of mineral nutrition in the soil . By comparison with ion uptake the
effort to understand these processes at the mechanistic level is meager. Perhaps
the successful use of fertilizers in agriculture has dulled our perceptions of what
is important in developing crop plants and cropping systems in difficult eco
nomic circumstances and in soils of lower fertility.
ACKNOWLEDGMENTS
I express . grateful thanks to my colleagues at Letcombe Laboratory (now

closed) and to V . Gianinazzi-Pearson, H. Lambers, J. A. Raven and P. B .
Tinker, who helped m e greatly by correspondence and discussion, and to Jean
Nash, who processed the manuscript with skill and speed .
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Factors Affecting Mineral Nutrient Acquisition Plants: Further

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Factors Affecting Mineral Nutrient Acquisition Plants: Further

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ANNUAL

The word acquisition emphasizes that more is involved in getting inorganic

isms or by free-living N-fixing microorganisms since these vigorous fields are

environment on nutrient acquisition. The discussion opens with results of

PROPERTIES OF THE ROOT SURFACE

distribution. The latter is a laborious matter to determine and very difficult

KINETIC PARAMETERS OF ION ABSORPTION In several models kinetic pa­

solutions follows a Michaelis-Menten relationship and can be used to derive

== Imax (Cs - Cmin)

where I max is the maximal inflow at high (saturating) levels of Cs

Cs == concentration at root surface

Cmin ==concentration at which there is no net inflow, i. e. In == °

This application of ion transport kinetics must have encouraged public­

diameter is by the development of root hairs.

ROOT HAIR DEVELOPMENT Several questions about the physiology and

the interesting suggestion that the quantitative significance of root hairs as a

WALL STRUCTURE/PERMEABILIT Y The outer wall surface o f root hairs

Modification of Rhizosphere Nutrient A vailability

ECOSEMANTICS There are large numbers of microbes in the rhizosphere

POLYSACCHARIDE SECRETIONS Polysaccharides of several kinds are pro­

develops around rice roots in anaerobic waters or muds. The diffusion of O2

ACID SECRETION Some species are recognized as being particularly effective

acquisition (74). Particulate CaHP04 and MnOz were demonstrably solubil­

ENZYME RELEASE Nutrient deficiency, usually P-deficiency, frequently

just as in T. subterraneum, but there was no evidence at all of any net

CONCLUSIONS The roots of some species are capable of modifying soil

The copper nutrition of citrus plants appears to be adversely affected by

Glomus Jasiculatus has been shown to translocate 35sol- into mycorrhizal

Fungal Injection and Phosphate Nutrition

attached to shaded or defoliated or high nitrogen status plants significantly

PHOSPHATE ABSORPTION BY FUNGAL H YPHAE AND M YCORRHIZAL

ROOTS Inorganic phosphate from the soil solution is absorbed by external

from other fungi and yeasts, it is likely to be a 2 proton/Pi symport depending

TRANSLOCATION OF Pi WITHIN HYPHAE Much of the Pi entering the hyphae

vacuoles contain large granules which by electron-probe microanalyses have

s 1 This value is somewhat larger than estimates based on Pj accumulation by

HOST-FUNGUS INTERACTION IN THE ARBUSCULE The relationship between

Host Matrix zone Fungus

Manipulation of Host-Fungus Association

sanguine view of improvements of the effectiveness of the associations . While

REGULATION OF NUTRIENT INTAKE

The properties of ion absorption systems reflect the nutritional environment in

matched by equivalent efflux, causes luxury accumulation . This may be useful

Short-term Modulation Related to Internal Concentration

Some apparently conflicting reports on the effects of internal nutrient status on

Longer-term Adjustment of Carrier Activity

Even if cytoplasmic ion concentrations are relatively stable, it is evident that

there was no change in Km ( 1 1 8 ) . In the same species, K+ stress induced first a

roots and shoots seem to be independent of external ion concentration ( 1 3 , 4 1 ,

above, this homeostasis can be achieved by adjustments to carrier activity and

Regulation by Efflux Control

substantial and probably regulated independently (103, 1 29). Early attempts by

Fluxes Through the Symplast

The Size of the Absorbing Surface

intake-a regulation imposed from outside the plant.

THE ENERGY COST OF MINERAL NUTRITION

Many who work in agricultural research find themselves hag-ridden by frisky

Broad Sense Costs

wt for protein turnover and 6-10 mg glucose d - I g - I dry wt for compartmenta­

from roots by exudation or leakage into the rhizosphere . Numerous estimates of

MYCORRHIZAS With a few exceptions , all plant families develop symbiotic

than uninfected roots. The proportion of total photosynthesis transported to the

The carbon cost of establishing VAM associations can often be seen as a

KINETIC PARAMETERS OF ION ABSORPTION In several models kinetic pa

This application of ion transport kinetics must have encouraged public

POLYSACCHARIDE SECRETIONS Polysaccharides of several kinds are pro

acquisition (74). Particulate CaHP04 and MnOz were demonstrably solubil

wt for protein turnover and 6-10 mg glucose d - I g - I dry wt for compartmenta

supplied with nutrients . Calculations of the carbohydrate demand in the synthe

MECHANISTIC ACCOUNTING In the absence of knowledge of the mecha

1 . Abbott, L . K . , Robson, A . D . 1982. The tems derived from it. In Endornycorrhi

33:389--408 Phosphorus uptake, storage and utiliza

504 transport in a tropical legume, Macroptil

studies of processes involved in phos ning, A. W . Robards, pp. 297-3 1 1 . Ber

1 28 . Macklon, A . E. S . , Sim , A . 1 98 1 . Cor 142. Nye, P. H . , Tinker, P. B . 1 977. Solute

1 86 . Szaniawski, R. K. 1 98 1 . Growth and Osmoregulation. Impact on Plant Pro

62:376-86 rhizosphere in Zea mays cultivar Seneca