Plant Ion Transport
Secondary article
Rainer Hedrich, Bayerische Julius-Maximilians-University, Würzburg, Germany
M Rob G Roelfsema, Bayerische Julius-Maximilians-University, Würzburg, Germany
Article Contents
. How to Survive in Pond Water?
. Life on Earth
Plant ion transport plays a key role in major physiological processes, such as nutrient uptake
and redistribution, movement, growth and microbe interaction. Changes in the activity
and density of ion-pumps, channels and carriers represent essential membrane-delimited
steps in these processes.
. Nutrient Uptake
. Carbon is Absorbed from the Atmosphere
. Long-distance Ion Transport
. Growth and Tropisms
. Living in a Community
. Ion Transport in Progress
How to Survive in Pond Water?
After eukaryotic organisms were invaded by cyanobacteria, the first primitive unicellular algae were formed. At this
point, these creatures became photoautotrophic and took
advantage of the CO2-rich atmosphere to generate their
own carbohydrates. New habitats could be colonized that
were previously unsuitable for growth. The availability of
nutrients in these environments differed tremendously
from the ‘Jurassic pond’ in which life had started. To
sustain growth, nutrients had to be captured from a habitat
that could be as poor in ion-content as pond water. Plants
developed mechanisms to survive in these hostile environments and learned to concentrate essential nutrients from
their surrounding.
Most nutrients are taken up by plants as ions, with the
exception of carbon. Carbon is taken up as CO2 by most
plants, although some water plants take advantage of the
high concentration of HCO32 available in their aqueous
environment. During photosynthesis, CO2 is converted
into low-molecular mass carbohydrates that form the basis
of cellular components. The synthesis of proteins and
nucleic acids, however, also requires the uptake of
inorganic nitrogen, phosphate and sulfate. These ‘macronutrients’ are mainly taken up in their oxidized anionic
form, but nitrogen is also taken up as NH41 . Anion uptake
is charge-balanced by the uptake of cationic macronutrients, such as K 1 , Ca2 1 and Mg2 1 . Metal ions such as
those of Fe, Mn, Cu and Zn are taken up only in limited
amounts (micronutrients) and incorporated in the prosthetic groups of enzymes.
Life on Earth
After colonizing land, higher plants faced problems caused
by their immobility. Strategies evolved to overcome
limitations in nutrient availability and water supply,
yielding plants that are characterized by heterotrophic
roots and photoautotrophic shoots. Solvent and solute
uptake by the root is separated from CO2 assimilation in
the shoot. As a consequence, a complex network for
transport of ions, water and photoassimilates had to be
formed. The long-distance transport pathway from the
roots to the shoot and vice versa comprises the xylem and
the phloem. The xylem transports mainly water and ions
from the roots to the leaves, while the phloem delivers
carbon skeletons and amino acids from photosynthetically
active cells (sources) to rapidly growing tissues (sinks).
Nutrient Uptake
In vascular plants, nutrients are taken up by the root
system and face as a first barrier the plasma membrane of
root cells. Generally, nutrients are taken up by root hair
cells which penetrate the soil via their growing tip. When
nutrients are available at high concentrations they also can
diffuse through the cell wall continuum (apoplast) of the
root. The diffusion in the root, however, is limited by a
radial layer of cells (endodermis), with cell walls largely
impermeable to ions. Here, ions have to be transported
across the plasma membrane and through the cytoplasm
towards the root stele.
H 1 pumps
The uptake of ions into roots, and plant cells in general, is
mediated by transporters in the plasma membrane. A large
quantity of, ions is subsequently sequestered in the
vacuole, the storage organelle of plant cells (Figure 1). Both
the plasma membrane and vacuolar membrane are
energized by proton (H 1 ) pumps. These membrane
proteins translocate H 1 from the cytoplasm to the cell
wall space (apoplast) or into the vacuole, by hydrolysing
high-energy phosphates. Owing to the positive charge of
protons, pump activity can be measured as a positive
(outward) electrical current across membranes (Figure 2a).
Proton pumps create both a concentration difference for
H 1 and an electrical potential difference (membrane
potential) that is negative at the cytoplasmic side.
Membrane potential changes towards more positive values
are referred to as depolarizations, negative going changes
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Plant Ion Transport
ATPases share an autoinhibitory domain at their Cterminus. A protein, classified as 14-3-3 binds to this
autoinhibitory domain and thereby can stimulate pump
activity. Within the vacuolar membrane two different H 1
pumps are present, a V-type ATPase and a pyrophosphatase. The V-type ATPase is a multisubunit H 1 pump,
while the pyrophosphatase is encoded by a single gene
(AVP) in A. thaliana. The latter pump hydrolyses
pyrophosphate (PPi) to transport H 1 .
Ion channels
Figure 1 Schematic diagram of ion pumps and channels in guard cells
superimposed on an A. thaliana stomate. Stomatal movement is associated
with ion transport. The following ion channels and pumps have been
identified in guard cells: (1) a hyperpolarization-activated calcium
conductance, that carries an inward Ca2 1 current; (2) outward rectifying
K 1 channel, which releases K 1 after depolarization (see Figure 2c); (3)
inward K 1 channel that facilitates K 1 uptake when the membrane
potential is hyperpolarized (Figure 2c); (4) the plasma membrane proton
pump utilizes ATP to drive H 1 extrusion, its activity hyperpolarizes the
membrane potential (Figures 2a and 2b); (5) mechanically activated ion
channels with selectivity for either Ca2 1 , K 1 or Cl 2 , which probably
represent tension sensors; (6) fast and slow anion channels that upon
activation release anions and depolarize the membrane potential (Figures 2b
and d); (7) and (8) the V-type H 1 ATPase and pyrophosphatase drive H 1
extrusion into the vacuole; (9) fast vacuolar channels (FV) are active at low
cytoplasmic Ca2 1 levels and conduct K 1 ; (10) K 1 -conducting VK
channels are active at an intermediate cytoplasmic Ca2 1 level; (11) at a
high cytoplasmic Ca2 1 concentration the outward rectifying slow vacuolar
(SV) channel is activated (Figure 4a), it conducts K 1 , Ca2 1 and anions to
some extent; (12) anion fluxes across the vacuolar membrane are facilitated
by a protein kinase-activated anion channel; (13) Ca2 1 -permeable
channels activate in a voltage-dependent manner, in response to inositol
triphosphate (IP3) or cyclic ADP-ribose (cADPR).
as hyperpolarizations. Plasma membrane H 1 ATPases
can transport H 1 against a large electrical potential
difference; membrane potentials as hyperpolarized as
2 240 mV have been reported. The potential difference
across the vacuolar membrane is smaller and most likely
ranges from 2 20 to 2 60 mV. Most plant cells maintain a
slightly alkaline cytoplasm, with a pH value close to 7.5.
The apoplast and vacuole are more acidic, with pH values
often ranging from 5 to 6. However, depending on the cell
type, these pH differences can be more pronounced.
The H 1 pump in the plasma membrane is classified as P
type ATPase, a group of transporters widely distributed
throughout different phyla (Palmgren and Axelsen, 1998).
In Arabidopsis thaliana H 1 ATPases are encoded by at
least 10 different AHA genes. Plasma membrane H 1
2
Ion channels are pores, most of which are selective for a
particular cation or anion while others discriminate less
between ion species. The movement of an ion through such
a channel is passive: the interaction between the ion and the
channel-protein does not determine its direction of flow.
However, ions are electrically charged and the ion current
through channels depends on the membrane potential. The
negative membrane potential thus allows uptake of cations
against their concentration gradient. The relation between
ion gradients and the electrical potential for an individual
ion species is defined by Nernst’s law; E(I) 5 RT/(zI F) ln([I]out/[I]in), where E(I) is the driving force for ion
movement, R is the gas constant, T is the absolute
temperature, zI is the charge of the ion, F is the Faraday
constant and [I] is the concentration of the ion. According
to this law, a membrane potential of 2 240 mV allows cells
to maintain a 104 times higher K 1 concentration inside
than outside the cell (e.g. 100 mmol L 2 1 K 1 inside root
cells and 10 mmol L 2 1 outside).
Although open channels can conduct ionic currents
irrespective of their direction, the process of opening
(gating) is often voltage dependent. Two types of voltagedependent K 1 channels are found in most plant cells,
conducting either an inward or an outward current, under
physiological conditions. The inward rectifying K 1
channels activate at hyperpolarized membrane potentials,
in Figure 2c negative of 2 155 mV. In the same cell, outward
rectifying K 1 channels activate at depolarized potentials.
K 1 channels represent the best-characterized group of
ion transporters, both on the functional and the molecular
levels. On the basis of sequence similarities, these channels
can be divided into six families (Figure 3a). K 1 -channel
families can be grouped according to the number of
transmembrane domains and K 1 -selective pores
(Figure 3b). Initially the Arabidopsis thaliana K 1 channels
AKT1 and KAT1 were cloned through complementation
of yeast mutants lacking K 1 transporters. Other members
belonging to the same families and AKT3 were found by
screens for homologous genes. KCO1 and SKOR1 were
recognized in an A. thaliana EST database while searching
for sequence homology to known K 1 channels. The SKT2
and SKT3 genes of Solanum tuberosum were discovered in
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Plant Ion Transport
Figure 2 Electrical properties of ion transporters in the plasma membrane of guard cells. (a) H 1 pump currents in Vicia faba protoplasts. Pump currents
decrease at more negative potentials, when the H 1 is transported against a larger electrical gradient (membrane potential, Vm). (From Lohse and
Hedrich R (1992) Planta 188: 206–214.) (b) Spontaneous changes of the free-running membrane potential (Em) of an A. thaliana guard cell. The
Nernst potential of K 1 was estimated at 2 80 mV for this cell. Efflux of K 1 therefore will occur when Em is at its most positive value ( 2 60 mV), while K 1
uptake occurs during the periods at which Em is most negative ( 2 180 mV). At times indicated by ., voltage clamp protocols similar to Figure 2c were
applied. (From Roelfsema and Prins (1998) Planta 205: 100–112.) (c) Whole-cell K 1 currents of an A. thaliana guard cell. Time-dependent activation of
outward and inward rectifying K 1 channels occurs at membrane potentials positive of 2 80 mV and negative of 2 155 mV, respectively. (d) Singlechannel currents of the fast anion channel GCAC1 from V. faba. Opening of anion channels causes stepwise increases of negative (inward) currents,
equivalent to anion efflux. The current level with all channels closed is indicated by C, that of open channels by Ox, where x stands for the number of open
channels. The open probability depends on the degree of membrane depolarization. (Modified after Schulz-Lessdorf (1996) PhD thesis University of
Hannover.)
an approach to find proteins interacting with the Cterminus of KST1, using the yeast two-hybrid system.
The AKT1 gene encodes an inward K 1 channel that is
expressed in roots. Plants with a disrupted AKT1 gene
exhibit reduced growth at low K 1 concentrations in the
root medium and in the presence of NH41 (Hirsch et al.,
1998). Apparently, the channel is involved in K 1
nutrition, but plants have alternative K 1 -uptake systems
that enable mutated plants to grow normally in a K 1 -rich
medium. As a consequence of the Nernst law, K 1 channels
cannot provide an uptake system that operates at K 1
concentrations much lower than 10 mmol L 2 1. Below this
concentration, threshold active transport systems (carriers) must secure K 1 uptake.
Carriers
Owing to the broad specificity of carriers, plant cells are
able to take up a wide range of ions. Some carriers utilize
the gradient of one ion to energize the uptake of another. In
the plant plasma and vacuolar membranes, most carriers
mediate proton-coupled transport. For cations such as
K 1 , carriers provide a high-affinity uptake system capable
of capturing K 1 from extracellular concentrations lower
than 10 mmol L 2 1. For Hordeum vulgare and A. thaliana,
K 1 -carriers named HAK (Santa-Maria et al., 1997) and
AtKUP were found to mediate K 1 uptake, even from
concentrations below 1 mmol L 2 1. The transcription of
some of these transporters is increased at low K 1
concentrations in the root medium, indicating a role for
these proteins in overcoming K 1 starvation.
Most of the micronutrients are also taken up by carriers.
Specific transporters for nutrients such as Mn, Fe, Cu, Co
and Zn have been identified (Fox and Guerinot, 1998). In
A. thaliana the transporters for Cu, Fe and NH41 are
encoded by COPT, IRT and AtAMT genes, respectively.
These plasma membrane transporters most likely mediate
cotransport of these cations with H 1 .
Carriers are essential for the uptake of anions against
their concentration gradient, since the negative membrane
potential does not support anion uptake via channels.
Similar to that of K 1 , the uptake of anions like NO32
divides into components with low and high affinity. In A.
thaliana, three genes encoding NO32 transporters have
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Plant Ion Transport
Figure 3 Clustering of cloned plant K 1 channels based on sequence similarity. (a) Cloned K 1 channels superimposed on fluorescent branching veins of
an A. thaliana leaf expressing green fluorescent protein fused to the SUC2-promoter. (Plants provided by N. Sauer, University of Regensburg; confocal laser
microscopy by R. Steinmeyer.) At least six families of K 1 channels can be distinguished. The KAT1 gene codes for an inward K 1 channel from
Arabidopsis thaliana, which is expressed in guard cells and flowers. KST1 is the Solanum tuberosum homologue to KAT1, while KAT2 is structurally
related to KAT1. The AKT1 family also encodes inward rectifying channels. AKT1 was cloned from A. thaliana and is involved in K 1 uptake of roots; SKT1 is a
related clone from S. tuberosum and ZMK1 originates from maize and is associated with auxin-induced growth of coleoptiles. Members of the AKT3 family
are preferentially expressed in vascular tissue and encode K 1 channels that are largely voltage independent. AKT3 was cloned from A. thaliana, ZMK2 from
maize, SKT2 from S. tuberosum, VFK1 from Vicia faba and SPICK1 and SPICK2 from Samanea saman. SKOR1 encodes an outward K 1 rectifying channel from
A. thaliana, which is expressed in xylem parenchyma cells. SPORK1 is a related S. saman gene. The group of KCO1-related genes encode Ca2 1 dependent outward channels of unknown function. KCO1 and KCO2 originate from A. thaliana and SPOCK1 from S. saman. The KCO3 channel also
originates from A. thaliana but differs from KCO1 and KCO2 in the number of transmembrane domains. K 1 channel genes from Hordeum vulgare
(HVKCH1) and Plantago media (PMKCH1 and 2) are not grouped into one of these families. (b) K 1 channels consist of a multiplication of two
transmembrane domains, indicating a common evolutionary base. Channels with two or six transmembrane domains have only one pore region, while
two pore regions are found in channels with four and eight transmembrane domains. Channels with eight membrane-spanning domains have so far only
been identified in animals (TWIG) and yeast (YKC1).
been identified. The NLT1 gene encodes a low-affinity
transporter and is constitutively expressed. The CHL1
transporter may be active in the low-affinity as well as in the
high-affinity range, while NRT2 encodes a high-affinity
transporter. The expression of CHL1 and NRT2 is induced
when roots are exposed to NO32 . In contrast, the
transcription of sulfate and phosphate transporters is
often enhanced in the absence of the substrate. In A.
thaliana, transporters for phosphate and sulfate are
encoded by the APT and AST genes.
Calcium transport and signalling
Owing to the importance of phosphate in cellular
processes, cytoplasmic Ca2 1 has to be maintained at
micromolar levels, otherwise calcium phosphate would
4
form an insoluble precipitate. Extracellular signals can
trigger transient and sustained changes in the cytoplasmic
Ca2 1 concentration that serve as an intracellular signal.
These signals include chemical, osmotic and mechanical
stimuli and are involved in Ca2 1 -dependent responses that
control nutrient uptake, movement, growth, differentiation, symbiosis and defence against pathogens (Trewavas,
1999).
Calcium ion is extruded from the cytoplasm to the
apoplast, the endoplasmic reticulum and the vacuole; in
these compartments the Ca2 1 concentration is in the
millimolar range. Ca2 1 extrusion is accomplished by
Ca2 1 ATPases and possibly by the CAX; encoded Ca2 1 /
H 1 antiporter present in the vacuolar membrane,
identified in A. thaliana. The Ca2 1 ATPases are either
calmodulin-insensitive or calmodulin-stimulated. The
calmodulin-insensitive pump is found in the vacuolar
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Plant Ion Transport
membrane only, while calmodulin-stimulated Ca2 1
pumps are present both in the plasma membrane and
vacuolar membrane. The latter pump type comprises
ACA-encoded Ca2 1 ATPases that have an autoinhibitory
domain at their N-terminus that binds calmodulin (Harper
et al., 1998). After binding calmodulin, the domain is
released and the pump is activated. Ca2 1 stimulates
calmodulin binding and thereby regulates the activity of
this type of pump.
In the search for channels involved in Ca2 1 signalling,
Ca2 1 -permeable channels have been described in vacuolar
membrane, endoplasmic reticulum and plasma membrane.
These channels release Ca2 1 into the cytoplasm upon
activation. In the vacuolar membrane, Ca2 1 conductances
were reported that activate in response to inositol triphosphate (IP3) and cyclic ADP-ribose (cADPR) (Allen et al.,
1995) coexisting with voltage-dependent Ca2 1 channels.
The endoplasmatic reticulum, another Ca2 1 store, harbours a voltage and Ca2 1 gradient-sensitive Ca2 1
channel. The plasma membrane contains both voltagedependent (Grabov and Blatt, 1998) and mechanosensitive
Ca2 1 channels.
Sodium toxicity
The selectivity of transporters in the plasma membrane is
limited and uptake of toxic ions may occur. This is the case
for the micronutrient Na 1 , which is present at large
concentrations in the marine environment but at only
moderate quantities in most soils. Land plants benefit from
low concentrations of Na 1 , but higher concentrations
inhibit the growth of many crops. In irrigated soils the
Na 1 content often reaches toxic levels, which complicates
agriculture in these areas. Plants have developed different
strategies to overcome Na 1 toxicity. Plants sequester
Na 1 into their vacuole through a Na 1 /H 1 antiporter in
the vacuolar membrane, which in A. thaliana is encoded by
AtNHX. Alternatively, plants extrude Na 1 , either from
their roots or by specialized salt glands from their leaves.
The HKT1 transporter of A. thaliana couples Na 1 and
K 1 influx, when expressed in nonplant systems. Based on
these results, HKT1 was hypothesized to present a
mechanism to overcome Na 1 toxicity (Rubio et al.,
1995), although this role has been challenged. Salt
tolerance in A. thaliana, however, has been shown to
depend on a calcineurin-like protein phosphatase. In the
presence of this protein phosphatase, plants were able to
accumulate K 1 selectively from media high in Na 1 , in a
Ca2 1 -dependent manner (Liu and Zhu, 1998).
Carbon is Absorbed from the
Atmosphere
To prevent excessive loss of water, plants developed a waxy
layer, the cuticula, covering the shoot. This polymer is
impermeable to both H2O and CO2 and therefore also
limits CO2 absorption. To control water loss on one side
and enable CO2 assimilation on the other, microscopically
small pores in the leaf epidermis evolved, the stomates.
Stomates of C3 and C4 plants open in the light when CO2 is
required for photosynthesis, but close when CO2 concentrations in the leaf increase. The plant hormone abscisic
acid (ABA) mediates the response of stomates to a limited
water supply. During drought, the concentration of this
hormone increases, forcing stomates to close and reducing
transpiration. The hormone indole-3-acetic-acid (IAA)
has the opposite effect and stimulates stomatal opening,
when IAA-induced growth requires increased CO2-fixation.
Stomatal movement is based on ion transport
Opening and closure of stomates results from volume
changes of the two guard cells that surround the stomatal
pore (Figure 1). These guard cells swell or shrink in response
to changes in their osmotic content. Modulation of the
ionic content in the two motor cells changes the extent to
which they are pushed apart and thereby adjusts the
stomatal aperture. The changes in osmotic content are
largely due to uptake and release of K 1 salts. During
stomatal opening, guard cells take up K 1 and Cl 2 and
convert starch into the organic anion malate.
Guard cells utilize ion channels both for the uptake and
for the release of K 1 ions. This is enabled by changes in the
membrane potential (Figure 2b). At depolarized membrane
potentials, K 1 is extruded via outward channels, while
K 1 is taken up via inward channels at hyperpolarized
membrane potentials (Figure 2c). The hyperpolarized
membrane potentials result from H 1 ATPase activity,
while anion channel activity depolarizes the membrane
potential. Two types of anion channels are present in the
plasma membrane that differ in activation velocity and are
referred as rapid (R-type) and slow (S-type) anion
channels. Both channels activate upon depolarization;
the threshold for the R-type channel is around 2 120 mV
(Figure 2d). Anion channels in the plasma membrane of
guard cells as well as in other plant and animal cells
conduct Cl 2 and NO32 as well as small organic acids.
During stomatal closure, these channels facilitate Cl 2 and
malate efflux from guard cells (Keller et al., 1989).
Changes in the activity of H 1 ATPases and anion
channels can alter the direction of the ion fluxes across the
plasma membrane, owing to their effects on the membrane
potential. Light, CO2 and hormones affect the activity of
these two transporters and the activity of K 1 channels.
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Plant Ion Transport
Both red and blue light (Assmann et al., 1985) stimulate the
activity of H 1 ATPases and trigger stomatal opening. CO2
has the opposite effect and triggers stomatal closure. This
CO2 response may be mediated by malate since apoplastic
malate reflects the ambient CO2 concentration. Extracellular malate activates the Ca2 1 -dependent R-type
anion channels and triggers stomatal closure. The CO2
response also involves an increase in cytoplasmic Ca2 1 , or
triggers Ca2 1 oscillations, in guard cells of Commelina
communis (Webb et al., 1996). Comparable increases in
cytoplasmic Ca2 1 were evoked by ABA and IAA,
although these hormones have opposite effects on stomatal
movement. The precise role of the increase in cytoplasmic
Ca2 1 in regulating stomatal movement is therefore still
under debate.
In addition to voltage-dependent channels, mechanically activated ion channels are present in the guard cell
plasma membrane that provide sensors for the membrane
tension. Three stretch-activated channels have been
identified that are selective for either K 1 and Cl 2 or
Ca2 1 (Cosgrove and Hedrich, 1991).
A number of ion channels in guard cells are regulated
through changes in the cytoplasmic Ca2 1 concentration.
In the plasma membrane of guard cells, both the R-type
and S-type anion channels are Ca2 1 stimulated. In the
same cell type, the conductance of the inward K 1 channel
is reduced by cytoplasmic Ca2 1 . In the vacuolar membrane, three types of Ca2 1 regulated K 1 -permeable
channels have been identified (Figure 1). The FV channels
are inhibited by cytoplasmic Ca2 1 , VK channels are active
at intermediate Ca2 1 levels and the SV-type channel is
Ca2 1 -stimulated (Hedrich and Neher, 1987; Figure 4a).
Most of these channels are also sensitive to changes in the
cytoplasmic pH. In the plasma membrane of guard cells,
cytoplasmic acidification stimulates the inward K 1
channel and inhibits the outward K 1 channel. The inward
K 1 channel also is affected by changes in the extracellular
pH; acidification stimulates this channel (Figure 4b)
through a shift in the voltage dependence. The pH sensor
of the KST1 channel is based on two histidine residues
located on the extracellular face of the channel (Hoth et al.,
1997).
A. thaliana mutant analysis has revealed that guard cell
responses to ABA involve protein farnesylation and
phosphorylation. In guard cells, ABA affects K 1 channels, stimulates S-type anion channels and inhibits H 1
extrusion. These ABA responses were absent in guard cells
expressing mutated ABI1 and ABI2 genes, while guard cells
lacking a functional farnesyltransferase are ABA hypersensitive (Pei et al., 1998).
Long-distance Ion Transport
Nutrients taken up by root cells may be transported
towards the stele via plasmodesmata that interconnect the
cytoplasm of adjacent cells. Finally, the nutrients are
extruded into xylem vessels by xylem parenchyma cells.
The ionic flow into xylem vessels is followed by an
osmotically driven flow of water into the vessels, thereby
creating the root pressure. As a result, a unidirectional flow
of water and ions through the xylem vessels develops, that
mediates long-distance nutrient transport from the root to
the shoot. The flow is enhanced by the evaporation of water
from stomatal pores in the leaves, that create a tension for
water flow through xylem vessels. In xylem parenchyma
cells the SKOR1 channel is expressed, encoding an
outward K 1 channel. Mutants of A. thaliana lacking this
channel are impaired in K 1 transport into the xylem
vessels, which results in a lower K 1 concentration of their
shoots (Gaymard et al., 1998). During drought, expression
of the SKOR1 channel is reduced by ABA, resulting in a
lower conductance of outward K 1 channels in xylem
parenchyma cells.
Sieve tubes mediate a phloem solute flow in the opposite
direction, providing roots with carbohydrates and amino
acids. In addition, the phloem serves growing parts of the
Figure 4 Regulation of ion channels by Ca2 1 ions and protons. (a) The SV
channel is regulated by cytoplasmic Ca2 1 . At 80 mV the steady-state
current increases upon elevation of cytoplasmic Ca2 1 concentrations.
(From Hedrich and Neher, 1987). (b) The inward K 1 channels of A.
thaliana guard cells are regulated by extracellular pH. Acidification
increases the current carried by the inward K 1 channel at 2 200 mV. (From
Brüggemann et al. (1999) Planta 207: 370–376.)
6
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Plant Ion Transport
shoot such as developing leaves and flowers. The phloem is
also important for the redistribution of K 1 . The xylem
transports large quantities of K 1 to the leaves that would
be concentrated owing to the evaporation of water if the
phloem did not transport ions back to the roots. The
mechanism sustaining the phloem ion transport is unknown, but VFK1 encoding a K 1 channel with homology
to AKT3 is preferentially expressed in sink tissues of the
shoot. The AKT3 channel is expressed in phloem
companion cells and encodes a weakly voltage-dependent
channel that is blocked by extracellular H 1 (Marten et al.,
1999).
Growth and Tropisms
The marine environment, in which life developed, had a
high salinity and allowed cells to maintain a large
concentration of osmolytes within their cytoplasm. Later,
plants encountered more dilute environments and took
advantage of a ridged cell wall to prevent uncontrolled
osmotic swelling. The pressure by which the plasma
membrane pushes against the cell wall is termed turgor.
Nonwoody plants gain their mechanical stability from this
interaction. Furthermore, the turgor drives the expansion
of growing cells.
During growth, cell walls become extensible and cells
swell through the uptake of ions and water, followed by de
novo synthesis of membranes and cell wall. The cell wall
extensibility is regulated by expansins, acid-stimulated
proteins. Stimuli like light and IAA can induce acidification of the cell wall and trigger cell growth. Acid growth of
cells is accompanied by activation of H 1 ATPases and
several ion channels. The growth response of maize
coleoptiles, triggered by IAA, involves transcriptional
regulation of the K 1 channel ZMK1. Expression of
ZMK1, a K 1 -uptake channel gene homologous to AKT1
(Figure 3), correlates with coleoptile elongation (Philippar
et al., 1999). Upon gravistimulation, auxin redistributes
between the upper and lower half of the coleoptile. An
increase of ZMK1 expression in the lower half and a
decrease in the upper precedes the upward bending of this
organ. Apparently, the auxin response involves an increase
of K 1 channel density. Hormonal control of ion channel
transcription was also described for SKOR1 (see above).
A growth pattern different from cell elongation is found
in Fucus rhizoids, root-hair and pollen-tube cells, which
display tip-growth. In Fucus rhizoids, mechanically
activated channels can increase Ca2 1 concentrations in
the rhizoid tip. Growth in all three cell types is reflected by a
Ca2 1 gradient from the growing tip towards the base of the
cell. Changes in growth direction can be evoked by
mechanical and chemical stimuli and are accompanied by
a change in the Ca2 1 gradient. These Ca2 1 gradients
enable root hairs to grow away from the root and around
objects in their way, while pollen tubes are guided towards
the oocytes by a largely unsolved chemical messenger
mechanism.
Living in a Community
Within their natural habitats, plants interact with many
different organisms. Often these interactions are disadvantageous to the plant, as they are affected by animals, fungi
or bacteria. Plants have mechanisms to defend themselves
against pathogens. Some pathogens are recognized by
plant cells through messengers, called elicitors, extruded by
the pathogen. These elicitors were found to activate Ca2 1
channels in the plasma membrane of tomato and parsley
cells (Zimmermann et al., 1997). Subsequently, the elicitorevoked rise in cytoplasmic Ca2 1 mediates a defence
response to the pathogen.
Some interactions with microorganisms, however, are
beneficial and stimulate plant growth under certain
conditions. Most common are symbiotic interactions with
soil fungi, called mycorrhiza. Mycorrhiza penetrate the soil
over large distances and provide the plant root with
nutrients that are scarce in the soil. The fungi benefits from
carbohydrates released by the roots. Plants have developed
mechanisms to recognize nitrogen-fixing bacteria that
enable them to grow on soils poor in fixed nitrogen. Their
roots associate with bacteria such as Azoarcus or
Azospirrilum that produce NH41 using the N2 that is
readily available. In tomato, the LeAMT2 transporter is
induced by NH41 and nitrogen-fixing bacteria, providing
an uptake mechanism for NH41 .
A more intense interaction occurs between Rhizobia and
roots of certain plant species. Here, the plant root forms a
structure, called nodule, to host the bacteria within the
root. The Rhizobia bacteria are surrounded by the
peribacteroid membrane in which specialized transport
proteins are present. In this membrane an NH41 -permeable channel was identified (Tyerman et al., 1995) that
transports the NH41 produced by the bacteria towards the
sites of amino acid synthesis in the root.
Endosymbiosis represents a tight interaction between
microorganisms and cells. Chloroplasts most likely originate from an endosymbiotic interaction. Following the
invasion of plant cells by cyanobacteria, this green
symbiont evolved into the photosynthetic organelle. This
hypothesis is supported by the finding that protein
transport proteins and K 1 channels of chloroplasts are
closely related to that of the cyanobacteria Synechocystis.
Ion Transport in Progress
The molecular structure of Ca2 1 -permeable channels
expressed in the plasma membrane and vacuolar mem-
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
7
Plant Ion Transport
branes remains as yet unknown. These channels will
probably be identified either by homology to an L-type
like channel of yeast or by functional complementation of
the respective yeast mutant. Chloride channels have been
identified in an approach as outlined above, but these
channels so far lack functional expression in heterologous
systems.
So far, most of the ion channels cloned have been
voltage-dependent, with the exception of the AKT3
channel family, which is blocked by protons but largely
voltage-insensitive. Genes encoding channels activated by
ligands, which are commonly found in animal cells, have so
far not been isolated in plants. Recently, however,
sequences with similarity to the channels binding glutamate and cyclic nucleotides have been found for plants.
These newly identified genes offer intriguing new areas for
research in ion transport and signalling processes of plants.
Their animal counterparts have functions in the brain or
sensory cells of the retina; tracking the function of these
genes in plants may therefore answer questions about how
plant cells communicate.
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