Chapter | 2 Ion Uptake Mechanisms of Individual Cells and Roots: Short-distance Transport
particular root temperature and include adaptive responses,
for example changes in root membrane properties. The
latter effects are of greater ecological significance. Such
studies often compare plants exposed to different root tem-
peratures, but the same shoot temperature. This creates a
temperature differential between the root and the shoot,
and it is noteworthy that the shoot meristem of, for exam-
ple, gramminoid plants is close to stem base. Thus, differ-
ent temperatures in the rooting medium will influence cell
division and cell elongation in the shoot. In the long term,
such experimental systems can affect the growth rates of
root and shoot quite differently and, thus, the root/shoot
biomass ratio (Clarkson et al., 1988, 1992). Accordingly,
long-term effects of root temperature on ion uptake can
include feedback regulation via plant demand, an example
of which is shown for maize in Table 2.12.
In maize, low root temperatures (12°C) decrease shoot
and root growth and uptake rates of nitrate and potassium,
as might be expected for a cold-sensitive plant species.
However, the reduction in ion uptake at low tempera-
ture was not a temperature effect on the roots per se, but
reflected feedback regulation via lower shoot demand.
This was shown by increasing the temperature of the shoot
growing zone (stem base) (24/12°C). Shoot growth was
strongly increased (i.e., the demand for nutrients) and so
were the uptake rates of nitrate and potassium per unit root
weight (Table 2.12). Similarly, in other graminaceous spe-
cies, poor growth at low root temperatures is generally not
caused by limited uptake of nutrients such as N, K or P
(Clarkson et al., 1986, 1992).
Low root temperatures can affect the uptake of nutri-
ents differently, P uptake usually being reduced more than
the uptake of other nutrients (e.g., Engels and Marschner,
1992a; Engels, 1993). The uptake rate of nitrate seems to
be more strongly reduced at low root zone temperatures
TABLE 2.12 Shoot and root growth and uptake of
nitrate and K by maize plants grown at different root
zone temperatures (RZT) and the temperatures at the
stem base (shoot growing zone temperature, SGT) for
eight days
Temperature treatment
(SGT°C/RZT°C)
24/24 12/12 24/12
1
Shoot growth (g fw day ) 1.91 0.32 1.34
Root growth (g fw day1) 0.85 0.20 0.26
Nitrate uptake (pmol g1 fw day1) 6.40 4.20 7.60
K uptake (pmol g1 fw day1) 2.50 1.20 3.10
After Engels and Marschner (1992a).
25
than ammonium in cold-sensitive plants like cucumber
(Tachibana, 1987), and in cold-tolerant species, such as
barley and ryegrass, the strong preference for ammonium
compared with nitrate uptake is little affected by the tem-
perature of the root zone (Macduff and Jackson, 1991;
Clarkson et al., 1992). Compared with Ca and Mg, uptake
rates of K are often more affected by root zone tempera-
tures. In winter wheat, the increase in K/(Ca  Mg) ratios
in the shoots with increasing root zone temperature may
cause tetany in grazing beef cattle on winter wheat forage
(Miyasaka and Grunes, 1990).
In contrast to plants grown in solution culture, the
roots of plants grown in soil must forage for many immo-
bile nutrients (Engels and Marschner, 1990; Rengel,
2001; Lynch, 2007; White and Hammond, 2008; White
and Broadley, 2009). In soil-grown plants, therefore, root
temperature can affect the uptake of nutrients additionally
through effects on root growth rate and root system mor-
phology (Section 13.3).
2.5.4 Interactions between Ions in the
Rhizosphere
In the preceding sections, for the sake of simplicity, the
transport of a particular ion was treated as a singular
process. In reality, however, the transporters catalysing ion
uptake are rarely specific and ions can compete directly
for transport. This competition is influenced by the proper-
ties of the transporter itself and by the concentrations of
different ions in solution. Solutes that are not transported
can also interact with transport proteins altering their activ-
ity. In addition, there may be indirect interactions between
ions as a result of their transport across the plasma mem-
brane, for example via effects on membrane potential
through the movement of charge, or via effects on the pro-
ton electrochemical gradient through the coupling of solute
transport to proton movements.
2.5.4.1 Competition
Transport proteins catalyse the movement of nutrients
from the rhizosphere solution to the cytoplasm across the
plasma membrane of root cells (Fig. 2.9). Competition
between ions of the same valency for entry to a chan-
nel protein or for binding to a carrier protein is common,
whether these ions are ultimately transported or merely
inhibit the transport process. Such competition occurs
particularly between ions with similar physicochemi-
cal properties (valency and ion diameter), for example
between the alkali cations potassium (K), rubidium
(Rb), cesium (Cs) and sodium (Na), or between the
Group II divalent cations calcium (Ca2), strontium (Sr2)
and barium (Ba2). It is important to note, however, that
the inhibition of transport of a particular ion by another ion
26 PART | I Nutritional Physiology

TABLE 2.13 Interactions between the uptake of NH4 TABLE 2.14 Uptake of labelled Mg2 (28 Mg) by barley
and K by maize rootsa seedlings without or with supply of K and Ca2
(0.25 mM each)
Concentration in roots (µmol g1 fw)
Ammonium Potassium Mg2 Uptake (µmol Mg2 (10 g)1 fw 8 h1)

(NH4)2SO4 (mM) K K K K MgCl2 

MgCl2 MgCl2  CaSO4 CaSO4  KCl
0.00 6.9 6.7 8.2 53.7
Roots 165 115 15.0
0.15 7.3 7.1 6.7 48.4
Shoots 88 25 6.5
0.50 17.1 13.5 8.9 41.1
Based on Schimansky (1981).
5.00 29.4 31.5 9.3 27.1
Based on Rufty et al. (1982a).
a
Duration of the experiment: 8 h;  K indicates addition of 0.15 mM K;
calcium concentration constant at 0.15 mM.
TABLE 2.15 Uptake rates of Mn and Mg by roots of
soybean plants at increasing Mn concentrations in the
does not necessarily imply that the inhibitory ion is itself substrate
transported. Manganese supply (µM)
Radioactive rubidium (86Rb) has often been used as a 1
Nutrient (μmol g root dw) 1.8 90 275
tracer to study K transport in plants, although this can
give misleading results under certain circumstances (Behl Mn 0.5 3.1 4.8
and Jeschke, 1982). In general, transport proteins catalys- Mg 121.8 81.1 20.2
ing K transport across the plasma membrane of root cells, Based on Heenan and Campbell (1981).
such as K-channels, cation-channels, and proton-coupled
K symporters, do not differentiate between K and
Rb for transport (White, 1997; Maathuis and Amtmann,
1999; Vallejo et al., 2005; Pyo et al., 2010; White and ammonium by root cells will be determined not only by
Karley, 2010). However, the major K-channel in roots of competition of NH4 for cation transporters, but also by
Arabidopsis thaliana (AtAKT1:AtKC1) is relatively imper- rhizosphere pH and cytosolic tolerance of NH4 and NH3
meable to Cs, which inhibits K influx through this uptake.
channel (White and Broadley, 2000). By contrast, proton- Applications of K and Ca fertilizers often induce Mg
coupled K symporters, such as AtHAK5, can transport deficiency in crop plants. This is partly a consequence of
both K and Cs into root cells and, in plants sufficiently cations, such as K and Ca2, inhibiting Mg2 uptake
supplied with K, the influx of both Cs and Na is thought by plant roots (Table 2.14). The presence of Mn2 in the
to occur largely through non-selective cation-channels rhizosphere also inhibits Mg2 uptake by roots (Table
(White and Broadley, 2000; Qi et al., 2008; Munns and 2.15), but has little effect on the uptake of K (Heenan and
Tester, 2008). Campbell, 1981). This presumably reflects the contrasting
The competition between potassium (K) and ammo- specificity of the transporters responsible for the uptake of
nium (NH4) is difficult to explain simply by competi- each cation.
tion for a single transport process at the plasma membrane Competition also occurs between anions for uptake by
(Table 2.13). Whereas NH4 is quite effective in inhibiting root cells. Some well-known examples are competition
K influx, the reverse (inhibition of NH4 uptake by K) between sulphate and molybdate, sulphate and selenate,
is rarely observed (e.g., Mengel et al., 1976; Rufty et al., selenite and phosphate, and phosphate and arsenate.
1982a; Shaviv et al., 1987). This may be explained by two Sulphate and molybdate are thought to enter root cells
phenomena. First, it has been reported recently that, in through the same proton-coupled symporters (Fitzpatrick
Arabidopsis thaliana, NH4 competes with K for trans- et al., 2008). Increasing the sulphate concentration in
port through both AtAKT1 and AtHAK5 (ten Hoopen the rooting medium reduces molybdate uptake strongly.
et al., 2010) and also reduces the expression of AtHAK5 Hence, S fertilization may be an effective tool to reduce
(Qi et al., 2008), whereas K does not appear to affect excessive Mo uptake thereby improving plant growth
the expression or activity of the major NH4 transporter, and animal nutrition in soils containing high concentra-
AtAMT1. Second, a substantial proportion of ammonium tions of Mo (Pasricha et al., 1977; Chatterjee et al., 1992).
may not be taken up as NH4 through transporters such as However, the competition may become a critical factor in
AtAMT1 but as NH3 (Section 2.5.2). Thus, the uptake of soils containing little Mo.
Chapter | 2 Ion Uptake Mechanisms of Individual Cells and Roots: Short-distance Transport
The interactions between selenate and sulphate are also
quite distinct, and of considerable practical importance in
view of the absolute requirement for selenium of humans
and animals and the detrimental effects of excessive sele-
nium in the diet (White and Broadley, 2005a, 2009).
Sulphate and selenate are taken up into root cells through
the same proton-coupled symporters (White et al., 2007b).
Increasing sulphate concentration in the substrate strongly
decreases selenate uptake by roots and selenium accumu-
lation by plants, suggesting direct competition between
selenate and sulphate for transport (White et al., 2007b).
On the other hand, increasing selenate concentration in the
substrate often increases sulphate uptake and accumulation
by plants (White et al., 2004, 2007b; Stroud et al., 2010),
possibly by interfering with the regulation of expression
or activity of high-affinity sulphate transporters by plant
S-status (White et al., 2004, 2007b).
Antagonistic interactions between selenite and phos-
phate, and also between phosphate and arsenate, are
thought to occur because these anions are transported by
the same proton-coupled symporters into root cells (Li
et al., 2008c; Zhao et al., 2010). In Holcus lanatus L.,
arsenate-tolerant and non-tolerant genotypes exist, and
arsenate uptake is much lower in the tolerant genotypes
(Meharg and Macnair, 1992). The low arsenate uptake rate
is achieved by suppression of the P deficiency-induced
high affinity uptake system in the tolerant plants. Similar
mechanisms of arsenic tolerance have been observed in
other plant species. For example, mutants of Arabidopsis
thaliana with defective phosphate transport are more tol-
erant to arsenate (Shin et al., 2004). Arsenite and undis-
sociated methylated arsenic species are taken up by roots
through the silicon transport pathway via members of the
nodulin 26-like intrinsic protein (NIP) family (Zhao et al.,
2010). Members of this family also transport a range of
small neutral molecules including ammonia, urea, boric
acid and silicic acid (Maurel et al., 2008; Wallace et al.,
2006; Miwa and Fujiwara, 2010).
The inability of transport proteins to differentiate effec-
tively between K and Rb, Ca2 and Ba2, SO42 and
SeO42, and phosphate and arsenate illustrates that the
selectivity of transport proteins in the plasma membrane of
root cells does not indicate any essential role for an ele-
ment in the plant, but merely reflects the physicochemi-
cal similarities between ions. Plant roots may be unable
to exclude many non-essential or toxic ions from the root
symplasm. This has important practical implications,
for example, for the entry of heavy metals into the food
chain via their uptake and accumulation by plants (e.g.,
Marschner, 1983).
Another distinct type of anion competition occurs
between chloride and nitrate. Chloride concentrations
in plant tissues, particularly in roots, can be reduced
strongly by increasing nitrate availability (Table 2.16).
27
TABLE 2.16 Chloride concentrations in roots
and shoots of barley plants at different nitrate
concentrations in the nutrient solution
Concentation in Chloride content
nutrient solution (mM) (µmol g1 fw)
Cl NO3 Roots Shoot
1 0 52 93
1 0.2 26 73
1 1.0 13 54
1 5.0 9 46
Based on Glass and Siddiqi (1985).
This reduction seems to be the result of negative feedback
from nitrate stored in the vacuoles of root cells (Glass and
Siddiqi, 1985). Similarly, nitrate uptake is reduced when
roots contain high chloride concentrations, and chlo-
ride accumulated in the vacuoles seems to be particularly
effective in this respect (Cram, 1973). The active efflux of
chloride and nitrate from the cytoplasm into the vacuole is
catalysed, in part, by the same proton-coupled transporters
(members of the CLC family) and several anion channels
also facilitate the movement of both Cl and NO3 across
the tonoplast (White and Broadley, 2001; Martinoia et al.,
2007; Teakle and Tyerman, 2010; Zifarelli and Pusch,
2010). Thus, it is possible that the two anions compete for
transport across the tonoplast, which affects their accumu-
lation in vacuoles, cytoplasmic concentrations and uptake.
In addition, several anion channels and proton-coupled
symporters in the plasma membranes of root cells appear
to facilitate the transport of both chloride and nitrate
(White and Broadley, 2001; Roberts, 2006), suggesting
further interactions in the pathways of their uptake and
accumulation.
Interactions between nitrate and chloride during their
uptake and accumulation in vacuoles are of great impor-
tance for crop production. The competing effect of chlo-
ride can be used to decrease the nitrate content of plant
species such as spinach which tend to accumulate large
amounts of nitrate for use as an osmoticum. On the other
hand, in saline soils, the competing effect of chloride on
nitrate uptake may impair N uptake by the plants (Bernal
et al., 1974). Under these conditions increasing nitrate sup-
ply can be an effective means to improve the N nutritional
status of the plants and simultaneously prevent chloride
toxicity in sensitive plant species (Section 17.6).
An interesting case of the indirect regulation of trans-
port by nutrients is the inhibition of nitrate uptake, and
stimulation of chloride uptake, by ammonium supply
(Lee and Drew, 1989; Xu et al., 2000; Miller and Cramer,
28 PART | I Nutritional Physiology

2004). In almost all cases, increasing the availability of
ammonium strongly suppresses nitrate uptake. By contrast,
increasing nitrate supply generally has little or no effect on
ammonium uptake (Breteler and Siegerist, 1984). Thus,
when nitrogen is supplied as NH4NO3, ammonium is taken
up in preference to nitrate. In Norway spruce, the rhizo-
sphere ammonium concentration must fall below about
100 µM NH4 before nitrate uptake occurs (Marschner
et al., 1991). In short-term experiments with barley, exter-
nal ammonium inhibited net influx of nitrate within 3 min,
and upon removing ammonium from the external solution
net influx of nitrate resumed within 3 min (Lee and Drew,
1989). Such immediate effects suggest that they arise from
the effect of ammonium on the electrochemical gradients
supporting nitrate uptake across the plasma membrane.
2.5.4.2 Effects of Extracellular Calcium
An example of synergism, first discovered by Viets (1944),
is the stimulation of cation and anion uptake by extracel-
lular Ca2 at low rhizosphere pH (Table 2.17; Fig. 2.17).
It is thought that this phenomenon is the result of Ca2
counteracting the negative effects of high H concentra-
tions on plasma membrane integrity or the activity of the
plasma membrane H-ATPase. Calcium, as a divalent
cation, stabilizes membranes through interactions with
the negatively charged headgroups of phospholipids and,
thereby, influences membrane function. It also contributes
to the resealing of the plasma membrane following dam-
age (Schapire et al., 2009). These functions of Ca2 are
reflected, for example, in the higher rates of efflux of low-
molecular-weight solutes across the plasma membrane of
Ca-deficient cells when faced with environmental chal-
lenges, such as low temperatures or mechanical damage.
Calcium can be removed fairly readily from its binding
sites at the outer surface of the plasma membrane, for
example by chelators (Van Steveninck, 1965), or can be
exchanged by high concentrations of H or metal cations
including Na (Lynch et al., 1987), which will increase
solute efflux.
Rhizosphere Ca2 concentration also influences the
selectivity of ion uptake, and the relative accumulation
of K and Na in particular. For example, in the absence
of Ca2 there are clear differences in the K/Na uptake
ratio between the ‘natrophobic’ maize and the ‘nat-
rophilic’ sugar beet. However, the presence of Ca2 in
the rhizosphere solution shifts the uptake ratio in favour
of K at the expense of Na in both species (Table 2.18).
These shifts in K/Na uptake ratio are likely to be due
to the fact that extracellular Ca2 inhibits Na influx
through voltage-insensitive cation-channels (White, 1999;
Maathuis and Amtmann, 1999; Munns and Tester, 2008),
but has little effect on K influx through inward-rectifying
K-channels (White, 1997a; Maathuis and Amtmann,
1999). High Ca2 concentrations in the soil solution are
particularly beneficial for the maintenance of high K/Na
uptake ratios in saline environments as they increase plant
salt tolerance.

TABLE 2.17 K and Cl uptake in barley roots with or 2.5.4.3 Cation–Anion Relationships
without Ca2 supply with external pH 5.0
The uptake of cations and anions occurs through differ-
Uptake rate (µmol g1 dw (2 h) 1) ent transport proteins (Fig. 2.9), therefore direct inter-
External K net Cl net actions between cations and anions for uptake are rare.
solution (mM) K influx uptake Cl influx uptake However, the uptake of one nutrient can influence the
uptake of another indirectly through effects on the mem-
0.1 KCl 116  3 117  6 35  1 34  4
brane potential, the proton electrochemical gradient or via
0.1 KCl  137  2 140  7 53  3 52  4 feedback regulation through plant growth or metabolism.
1.0 CaSO4 The stimulation of cation uptake by anions, and of anion
uptake by cations, is observed frequently, and is generally

TABLE 2.18 K/Na selectivity of roots with or without Ca2 supply

Uptake rate (µmol g1 fw (4 h) 1)
Maize Sugar beet
External solution NaCl 
KCl (10 mM each) Na K Na  K Na K Na  K
Ca 9.0 11.0 20.0 18.8 8.3 27.1

1 mM CaCl2 5.9 15.0 20.9 15.4 10.7 26.1