12 Mineral Nutrition of Higher Plants

minor fraction of the K+

(42
K) is readily exchangeable within this 30-min period, most
of the K+
having already been transported across the membranes into the cytoplasm
and vacuoles ('inner space').
Although the plasma membrane and the tonoplast are the main biomembranes
directly involved in solute uptake and transport in roots, it must be borne in m
ind that
compartmentation by biomembranes is a general prerequisite for living systems (L
eigh
and Wyn Jones, 1986). Solute transport into organelles such as mitochondria and
chloroplasts must also therefore be regulated by membranes which separate these
organelles from the surrounding cytoplasm. An example of solute transport across
the
outer chloroplast membrane is given in Section 8.4 for phosphorus and sugars.
The capability of biomembranes for solute transport and its regulation is closel
y
related to their chemical composition and molecular structure. Before the mechan
isms
of solute transport across membranes are discussed in more detail (Sections 2.4
and
2.5), it is therefore appropriate to consider some fundamental aspects of the co
mposition and structure of biomembranes.
2.3 Structure and Composition of Membranes
The capacity of plant cell membranes to regulate solute uptake has fascinated bo
tanists
since the nineteenth century. At that time the experimental techniques available
limited the investigation of the process. Nevertheless, even by the early years
of the
twentieth century some basic facts of solute permeation across the plasma membra
ne
and tonoplast had been established, as for example of the inverse relationship b
etween
membrane permeation and the diameter of uncharged molecules and the rates at whi
ch
they permeate membranes. These ultrafilter-like properties of membranes have bee
n
confirmed more recently, at least in principle (Table 2.5).
Thus, in addition to the cell walls (Section 2.2.1) cell membranes are effective
barriers to solutes of high molecular weight. Most synthetic chelators such as E
DTA
(see also Table 2.4) and microbial siderophores as specific chelators of iron (S
ection
16.5) are of high molecular weight and their rate of permeation is restricted th
rough the
Table 2.5
Reflection Coefficient (?) of Some Nonelectrolytes
at the Cell Membranes of Valonia utricularisa
Compound db
Molecule radius (nm)
Raffinose 1.00 0.61
Sucrose 1.00 0.53
Glucose 0.95 0.44
Glycerol 0.81 0.27
Urea 0.76 0.20

"Based on Zimmermann and Steudle (1970). 6

1.00 indicates that the membranes are impermeable to the
solute; 0 indicates that the membranes are freely permeable
to the solute.
Ion Uptake Mechanisms of Individual Cells and Roots 13
Fig. 2.4 Model of a biomembrane with polar lipids and with either extrinsic or i
ntrinsic,
integrated proteins. The latter can cross the membrane to form 'protein channels
'.
plasma membrane of root cells. It is possible, therefore, to use high-molecularweight
organic solutes such as polyethyleneglycol at high external concentrations as ef
fective
osmotica in order to induce water deficiency (drought stress) in plants.
Molecules which are highly soluble in organic solvents, i.e. with lipophilic pro
perties,
penetrate membranes much faster than would be predicted on the basis of their si
ze.
The solubility of these molecules in the membrane and their ability to diffuse t
hrough
the lipid core of the membranes are presumably the main factors responsible for
the
faster permeation.
Membranes are typically composed of two main classes of compounds: proteins and
lipids. Carbohydrates comprise only a minor fraction of membranes. The relative
abundance of proteins and lipids can be quite variable depending on whether the
membrane is a plasma, mitochondrial, or chloroplast membrane (Clarkson, 1977).
Membranes also differ in diameter, for example in spinach from 10.5 nm (plasma
membrane) to 8.1 nm (tonoplast) and 6.3 nm (endoplasmic reticulum; Auderset etal
.,
1986). However, all biomembranes have some common basic structure as shown in a
model in Fig. 2.4.
Polar lipids (e.g. phospholipids) with the hydrophilic, charged head regions (ph
osphate, amino, and carboxylic groups) are oriented towards the membrane surface.
Protein molecules can be attached (extrinsic proteins), for example, by electros
tatic
binding to the surfaces as membrane-bound enzymes. Other proteins may be integra
ted
into membranes (intrinsic proteins), or traverse the membranes to form 'protein
channels' (transport proteins) which serve to function in membrane transport of
polar
solutes such as ions (Section 2.4).
Three polar lipids represent the major lipid components of membranes: phospholipids, glycolipids, and less abundant, sulfolipids (except in the thylakoid mem
branes of
chloroplasts, where they occur in substantial amounts). Examples of these polar
lipids
are shown below:
14 Mineral Nutrition of Higher Plants
QLI R1
/\/\/\/\A/\/ v
O-CH 2
-0-P-0-CH2-CH2-N+
(CH3)3
O"
Phosphatidylcholine (lecithin)
H n ^ 2
0 J\ H Oh^c

(Long chain polyunsaturated

fatty acids)
CH 2 R2
/Ny^As/V^NyN^O-CH a
CH2OH
OH/OH
OH H
Monogalactosyl diglyceride
o
CH2 --0"
\H O
OH/OH
OH H
Sulfoquinovosyl diglyceride
Another important group of membrane lipids consists of sterols, for example sistosterol:
-Sistosterol
Through their structural role in membranes sterols may indirectly affect transpo
rt
processes such as the activity of the proton pumping ATPase in the plasma membra
ne
(Sandstrom and Cleland, 1989). In agreement with this assumption the sterol cont
ent is
very low in endomembranes (e.g. endoplasmic reticulum) but may make up more than
30% of the total lipids in the plasma membrane (Brown and DuPont, 1989) and also
in
the tonoplast (Table 2.6). Despite these differences in lipids, the fatty acid c
omposition
of the phospholipids is similar in both membranes. The long-chain fatty acids in
polar
membrane lipids vary in both the length and degree of unsaturation (i.e. number
of
double bounds) which influence the melting point (Table 2.6).
Lipid composition not only differs characteristically between membranes of individual cells but also between cells of different plant species (Stuiver et aL, 1
978), it is
also strongly affected by environmental factors. In leaves, for example, distinc
t annual
variations in the levels of sterols occur (Westerman and Roddick, 1981) and in r
oots
both phospholipid content and the proportion of highly unsaturated fatty acids d
ecrease
Ion Uptake Mechanisms of Individual Cells and Roots 15
Table 2.6
Lipid and Fatty Acid Composition of Plasma Membranes and Tonoplasts from Mung Be
ana
Lipids
Plasma membrane
t??\ mg- 1
protein
Tonoplast
p??? mg- 1
protein
Phospholipids
Sterols
Glycolipids
1.29
1.15

0.20
1.93
1.05
0.80
Fatty acid
Fatty acid composition of the phospholipids
Melting Plasma
Chain point membrane
length (C) (% of total)
Tonoplast
(% of total)
Palmitic acid
Stearic acid
Oleic acid
Linoleic acid
Linolenic acid
Others
Ci 6
Cl 8
G b
^-18:1
r b
r b
^18:3
+62.8
+70.1
+ 13.0
-5.5
-11.1
35
6
9
21
19
10
39
6
9
22
20
4
"Based on Yoshida and Uemura (1986). Reprinted by permission of the American Soc
iety of Plant
Physiologists.
^Numeral to the right of the colon indicates the number of double bounds.
under zinc deficiency (Cakmak and Marschner, 1988c). In many instances changes i
n
lipid composition reflect adaptation of a plant to its environment through adjus
tment of
membrane properties. Generally, highly unsaturated fatty acids predominate in pl
ants
that grow in cold climates. During acclimatization of plants to low temperatures
an
increase in highly unsaturated fatty acids is also often observed (Bulder et al.
, 1991).
Such a change shifts the freezing point (i.e. the transition temperature) of mem
branes
to a lower temperature and may thus be of importance for maintenance of membrane

functions at low temperatures. It is questionable, however, to generalize about

the
effect of temperature on lipid composition of membranes. In rye, for example, wh
ich is
a cold-tolerant plant species, the proportion of polyunsaturated fatty acids in
the roots
decreased rather than increased as the roots were cooled (White et al., 1990b).
During acclimatization of roots to low temperatures synthesis of new membrane
proteins is also enhanced (Mohapatra et al., 1988) and phospholipids increase co
nsiderably (Kinney et al., 1987). Since phospholipids probably act as receptors for ph
ytohormones such as gibberellic acid, increasing responsiveness of membranes to gibber
ellic
acid at low temperatures may be related to these changes (Singh and Paleg, 1984)
.
The property of membranes in ion selectivity and lipid composition are often hig
hly
correlated as for example between chloride uptake and sterols (Douglas and Walke
r,
i983) and galactolipids (Section 16.6). Also the crop plant species bean, sugar
beet and
barley differ not only in the fatty acid composition of root membranes (Stuiver
et al.,
1978) but also considerably in the uptake of sodium (Section 10.2).
Alterations in the lipid composition of root membranes are also typical response
s to
changes in the mineral nutrient supply or exposure to salinity (Kuiper, 1980). O
f the
12 Mineral Nutrition of Higher Plants
minor fraction of the K+
(42
K) is readily exchangeable within this 30-min period, most
of the K+
having already been transported across the membranes into the cytoplasm
and vacuoles ('inner space').
Although the plasma membrane and the tonoplast are the main biomembranes
directly involved in solute uptake and transport in roots, it must be borne in m
ind that
compartmentation by biomembranes is a general prerequisite for living systems (L
eigh
and Wyn Jones, 1986). Solute transport into organelles such as mitochondria and
chloroplasts must also therefore be regulated by membranes which separate these
organelles from the surrounding cytoplasm. An example of solute transport across
the
outer chloroplast membrane is given in Section 8.4 for phosphorus and sugars.
The capability of biomembranes for solute transport and its regulation is closel
y
related to their chemical composition and molecular structure. Before the mechan
isms
of solute transport across membranes are discussed in more detail (Sections 2.4
and
2.5), it is therefore appropriate to consider some fundamental aspects of the co
mposition and structure of biomembranes.
2.3 Structure and Composition of Membranes
The capacity of plant cell membranes to regulate solute uptake has fascinated bo
tanists
since the nineteenth century. At that time the experimental techniques available

limited the investigation of the process. Nevertheless, even by the early years
of the
twentieth century some basic facts of solute permeation across the plasma membra
ne
and tonoplast had been established, as for example of the inverse relationship b
etween
membrane permeation and the diameter of uncharged molecules and the rates at whi
ch
they permeate membranes. These ultrafilter-like properties of membranes have bee
n
confirmed more recently, at least in principle (Table 2.5).
Thus, in addition to the cell walls (Section 2.2.1) cell membranes are effective
barriers to solutes of high molecular weight. Most synthetic chelators such as E
DTA
(see also Table 2.4) and microbial siderophores as specific chelators of iron (S
ection
16.5) are of high molecular weight and their rate of permeation is restricted th
rough the
Table 2.5
Reflection Coefficient (?) of Some Nonelectrolytes
at the Cell Membranes of Valonia utricularisa
Compound db
Molecule radius (nm)
Raffinose 1.00 0.61
Sucrose 1.00 0.53
Glucose 0.95 0.44
Glycerol 0.81 0.27
Urea 0.76 0.20
"Based on Zimmermann and Steudle (1970). 6
1.00 indicates that the membranes are impermeable to the
solute; 0 indicates that the membranes are freely permeable
to the solute.
Ion Uptake Mechanisms of Individual Cells and Roots 13
Fig. 2.4 Model of a biomembrane with polar lipids and with either extrinsic or i
ntrinsic,
integrated proteins. The latter can cross the membrane to form 'protein channels
'.
plasma membrane of root cells. It is possible, therefore, to use high-molecularweight
organic solutes such as polyethyleneglycol at high external concentrations as ef
fective
osmotica in order to induce water deficiency (drought stress) in plants.
Molecules which are highly soluble in organic solvents, i.e. with lipophilic pro
perties,
penetrate membranes much faster than would be predicted on the basis of their si
ze.
The solubility of these molecules in the membrane and their ability to diffuse t
hrough
the lipid core of the membranes are presumably the main factors responsible for
the
faster permeation.
Membranes are typically composed of two main classes of compounds: proteins and
lipids. Carbohydrates comprise only a minor fraction of membranes. The relative
abundance of proteins and lipids can be quite variable depending on whether the
membrane is a plasma, mitochondrial, or chloroplast membrane (Clarkson, 1977).
Membranes also differ in diameter, for example in spinach from 10.5 nm (plasma
membrane) to 8.1 nm (tonoplast) and 6.3 nm (endoplasmic reticulum; Auderset etal
.,
1986). However, all biomembranes have some common basic structure as shown in a

model in Fig. 2.4.

Polar lipids (e.g. phospholipids) with the hydrophilic, charged head regions (ph
osphate, amino, and carboxylic groups) are oriented towards the membrane surface.
Protein molecules can be attached (extrinsic proteins), for example, by electros
tatic
binding to the surfaces as membrane-bound enzymes. Other proteins may be integra
ted
into membranes (intrinsic proteins), or traverse the membranes to form 'protein
channels' (transport proteins) which serve to function in membrane transport of
polar
solutes such as ions (Section 2.4).
Three polar lipids represent the major lipid components of membranes: phospholipids, glycolipids, and less abundant, sulfolipids (except in the thylakoid mem
branes of
chloroplasts, where they occur in substantial amounts). Examples of these polar
lipids
are shown below:
14 Mineral Nutrition of Higher Plants
QLI R1
/\/\/\/\A/\/ v
O-CH 2
-0-P-0-CH2-CH2-N+
(CH3)3
O"
Phosphatidylcholine (lecithin)
H n ^ 2
0 J\ H Oh^c
(Long chain polyunsaturated
fatty acids)
CH 2 R2
/Ny^As/V^NyN^O-CH a
CH2OH
OH/OH
OH H
Monogalactosyl diglyceride
o
CH2 --0"
\H O
OH/OH
OH H
Sulfoquinovosyl diglyceride
Another important group of membrane lipids consists of sterols, for example sistosterol:
-Sistosterol
Through their structural role in membranes sterols may indirectly affect transpo
rt
processes such as the activity of the proton pumping ATPase in the plasma membra
ne
(Sandstrom and Cleland, 1989). In agreement with this assumption the sterol cont
ent is
very low in endomembranes (e.g. endoplasmic reticulum) but may make up more than
30% of the total lipids in the plasma membrane (Brown and DuPont, 1989) and also
in
the tonoplast (Table 2.6). Despite these differences in lipids, the fatty acid c
omposition
of the phospholipids is similar in both membranes. The long-chain fatty acids in

polar
membrane lipids vary in both the length and degree of unsaturation (i.e. number
of
double bounds) which influence the melting point (Table 2.6).
Lipid composition not only differs characteristically between membranes of individual cells but also between cells of different plant species (Stuiver et aL, 1
978), it is
also strongly affected by environmental factors. In leaves, for example, distinc
t annual
variations in the levels of sterols occur (Westerman and Roddick, 1981) and in r
oots
both phospholipid content and the proportion of highly unsaturated fatty acids d
ecrease
Ion Uptake Mechanisms of Individual Cells and Roots 15
Table 2.6
Lipid and Fatty Acid Composition of Plasma Membranes and Tonoplasts from Mung Be
ana
Lipids
Plasma membrane
t??\ mg- 1
protein
Tonoplast
p??? mg- 1
protein
Phospholipids
Sterols
Glycolipids
1.29
1.15
0.20
1.93
1.05
0.80
Fatty acid
Fatty acid composition of the phospholipids
Melting Plasma
Chain point membrane
length (C) (% of total)
Tonoplast
(% of total)
Palmitic acid
Stearic acid
Oleic acid
Linoleic acid
Linolenic acid
Others
Ci 6
Cl 8
G b
^-18:1
r b
r b
^18:3
+62.8
+70.1
+ 13.0
-5.5
-11.1
35

6
9
21
19
10
39
6
9
22
20
4
"Based on Yoshida and Uemura (1986). Reprinted by permission of the American Soc
iety of Plant
Physiologists.
^Numeral to the right of the colon indicates the number of double bounds.
under zinc deficiency (Cakmak and Marschner, 1988c). In many instances changes i
n
lipid composition reflect adaptation of a plant to its environment through adjus
tment of
membrane properties. Generally, highly unsaturated fatty acids predominate in pl
ants
that grow in cold climates. During acclimatization of plants to low temperatures
an
increase in highly unsaturated fatty acids is also often observed (Bulder et al.
, 1991).
Such a change shifts the freezing point (i.e. the transition temperature) of mem
branes
to a lower temperature and may thus be of importance for maintenance of membrane
functions at low temperatures. It is questionable, however, to generalize about
the
effect of temperature on lipid composition of membranes. In rye, for example, wh
ich is
a cold-tolerant plant species, the proportion of polyunsaturated fatty acids in
the roots
decreased rather than increased as the roots were cooled (White et al., 1990b).
During acclimatization of roots to low temperatures synthesis of new membrane
proteins is also enhanced (Mohapatra et al., 1988) and phospholipids increase co
nsiderably (Kinney et al., 1987). Since phospholipids probably act as receptors for ph
ytohormones such as gibberellic acid, increasing responsiveness of membranes to gibber
ellic
acid at low temperatures may be related to these changes (Singh and Paleg, 1984)
.
The property of membranes in ion selectivity and lipid composition are often hig
hly
correlated as for example between chloride uptake and sterols (Douglas and Walke
r,
i983) and galactolipids (Section 16.6). Also the crop plant species bean, sugar
beet and
barley differ not only in the fatty acid composition of root membranes (Stuiver
et al.,
1978) but also considerably in the uptake of sodium (Section 10.2).
Alterations in the lipid composition of root membranes are also typical response
s to
changes in the mineral nutrient supply or exposure to salinity (Kuiper, 1980). O
f the
//BIMx
//Copyright 2002-2013 Graphisoft SE All rights reserved

//Sat Nov 28 10:55:38 2015

//0.000 InitCore
Program directory is 'C:\Program Files\GRAPHISOFT\ArchiCAD 18\Add-Ons\BIMx\'
Incoming path is 'C:\Program Files\GRAPHISOFT\ArchiCAD 18\Add-Ons\BIMx\BIMx.ap
x'
//0.003 Shutdown
Shutting down core
//BIMx
//Copyright 2002-2013 Graphisoft SE All rights reserved
//Sat Nov 28 10:55:38 2015
//0.000 InitCore
Program directory is 'C:\Program Files\GRAPHISOFT\ArchiCAD 18\Add-Ons\BIMx\'
Incoming path is 'C:\Program Files\GRAPHISOFT\ArchiCAD 18\Add-Ons\BIMx\BIMx.ap
x'
//0.003 Shutdown
Shutting down core
//BIMx
//Copyright 2002-2013 Graphisoft SE All rights reserved
//Sat Nov 28 10:55:38 2015
//0.000 InitCore
Program directory is 'C:\Program Files\GRAPHISOFT\ArchiCAD 18\Add-Ons\BIMx\'
Incoming path is 'C:\Program Files\GRAPHISOFT\ArchiCAD 18\Add-Ons\BIMx\BIMx.ap
x'
//0.003 Shutdown
Shutting down core