ways of ion channel gating in plant cells · 2015. 4. 21. · ligand-gated ion channels bind...

Annals of Botany 86: 449±469, 2000doi:10.1006/anbo.2000.1226, available online at http://www.idealibrary.com on

REVIEW

Ways of Ion Channel Gating in Plant Cells

ELZBIETA KROL and KAZIMIERZ TREBACZ*

Department of Biophysics, Institute of Biology, Maria Curie-Skl/odowska University, Akademicka 19, 20-033 Lublin,
Poland
Received: 12 April 2000 Returned for revision: 7 May 2000 Accepted: 12 June 2000 Published electronically: 21 July 2000

that these

0305-7364/0

AbbreviatioA-9-C, anthralight; cADPRprotein kinasequilibrium pinositol triphoacid; OA, okadependent onand phosphoTMB-8, 8 (N

* For corre

A precise control of ion channel opening is essential for the physiological functioning of plant cells. This process istermed gating. Ion channel gating can be e�ected by ligand-binding, ¯uctuations in membrane potential, membranestretch and light quality. Modern electrophysiological and molecular-biological techniques have enabled thecharacterization and classi®cation of many ion channels according to their gating phenomena. Indications are thatgating mechanisms are complex and that individual ion channels can be regulated by a number of factors. In thispaper, gating mechanisms are reviewed following a standard classi®cation of ion channels based on permeability. Thegating of K�, Ca2� and anion channels in the plasma membrane, tonoplast and endomembranes of plant cells isdescribed. # 2000 Annals of Botany Company

Key words: Review, ion channel, ligand-gating, voltage-gating, stretch-gating, light-gating, plasmalemma, tonoplast.

INTRODUCTION

Ion channels are integral components of all membranes andthey can be viewed as dynamic ion transport systemscoupled via membrane electrical activities (White et al.,1999). Not only do they in¯uence membrane voltagethrough the ionic currents they mediate, but their activitiescan also be regulated by membrane voltage. Ion channelscan be divided into four `historically-based' groups accord-ing to gating mechanism: ligand-gated, voltage-gated,stretch-activated and light-activated. Ligand-gated ionchannels bind intracellular second messengers which pro-vide the essential links between external stimuli and speci®cintracellular responses (Leckie et al., 1998). Moreover,additional modulations by ATP or protons make thechannels capable of sensing changes in energy status oracid metabolism, respectively (Schulz-Lessdorf et al., 1996).Voltage-dependent channels appear optimally suited forelectrical signal transmission via membrane depolarization(e.g. through action potentials) and/or for signal trans-duction in response to changes in membrane potential(e.g. models investigating the coupling between membranepotential and voltage-dependent Ca2�-channels suggest

are engaged in intracellular signalling). They

0/090449+21 $35.00/00

ns: ABA, Abscisic acid; ABC, ATP binding cassette;cene-9-carboxylic acid; AP, action potential; BL, blue, cyclic ADP-ribose; CDPK, calmodulin-like domaine; DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethyl urea; E,otential; I, current intensity; IAA, indol-3-acetic acid; IP3,sphate; NPPB, (5-nitro-2-3-phenylpropylamino) benzoicdaic acid; PLC, phospholipase C; PKA, protein kinasecyclic AMP; PKC, protein kinase dependent on [Ca2�]cytlipids; PKG, protein kinase dependent on cyclic GMP;,N diethylamino) octyl-3,4,5-trimethoxybenzoate.

spondence. E-mail [email protected]

are also involved in membrane voltage stabilization, whichis critical for maintaining ionic gradients and nutritionalion ¯uxes. Stretch-activated ion channels serve as addi-tional speci®c transmembrane `receptors' co-existing withother cellular volume-sensing mechanisms. Light-activatedchannels are in fact ligand-gated, although a preciseindication of the ligands is not yet possible because theprocess of light signal transduction remains unclear. Thesechannels are distinguished particularly because of a specialimportance of light stimuli in plant signalling processes.

Modern biomolecular techniques reveal how complicatedthe processes controlling channel behaviour are. It becomesincreasingly apparent that the activity of a channel maydepend on the developmental and metabolic stage of thecell. Moreover, regulation of ion channels relies not only onthe channel proteins themselves, but also to a great extenton regulatory polypeptides, such as auxiliary b-subunits,cytoskeletal components, 14-3-3 proteins, phosphates,kinases, and G-proteins (Czempinski et al., 1999).

Jan and Jan (1997) recently reviewed receptor-regulatedion channels in excitable and nonexcitable animal tissues(G-protein-gated and cGMP-gated K� channels; voltage-gated K�-, Na�-, Clÿ-, Ca2� channels; voltage-insensitiveCa2� channels; Ca2�-activated K� channels; ligand-gatedCa2� channels). The activities of these channels are sensi-tive to external and internal signals that are mediated byreceptors for hormones and transmitters. There are alsoplant-derived elicitor-speci®c receptors, which are closelycoupled with plasma membrane ion channels important forsignal transduction in plant cells (Ward et al., 1995;Blumwald et al., 1998). Studies on receptor-regulated ionchannels suggest that they too are gated via G-proteins,either by direct protein-protein interaction or indirectly
by kinase (PKA, PKG, PKC)/phosphatase cascades or
# 2000 Annals of Botany Company

Czempinski et al., 1999).

TABLE 1. Plant responses controlled by ion channel regulation

Plant response Reference

Blue- and red-light induced phototropism Cho and Spalding, 1996; Ermolayeva et al., 1996, 1997; Elzenga and Van Volkenburgh, 1997a;Lewis et al., 1997; Parks et al., 1998; Suh et al., 1998

Leaf movement Kim et al., 1992, 1996; Stoeckel and Takeda, 1993, 1995; Moran, 1996; Mayer et al., 1997

Plant excitability Katsuhara and Tazawa, 1992; Thiel et al., 1993

Light-induced hypocotyl elongation Sidler et al., 1998

Light-induced transient membranepotential changes

Trebacz et al., 1994; Elzenga et al., 1995, 1997; Blom-Zandstra et al., 1997; SchoÈ nknecht et al.,1998; Szarek and Trebacz, 1999

Light-induced stomatal opening Kinoshita and Shimazaki, 1997; Suh et al., 1998

ABA-induced stomatal closure Armstrong et al., 1995; McAinsh et al., 1995, 1997; Schmidt et al., 1995; Ward et al., 1995;Li and Assmann, 1996; Blatt and Grabov, 1997a,b; Esser et al., 1997; MacRobbie, 1997;Mori and Muto, 1997; Pei et al., 1997, 1998; Grabov and Blatt, 1998a; Leckie et al., 1998;Li et al., 1998; Schwarz and Schroeder, 1998; Barbier-Brygoo et al., 1999

Plant hormone-induced responses Marten et al., 1991; Hedrich and Jeromin, 1992; Schumaker and Gizinski, 1993;Blatt and Thiel, 1994; Zimmermann et al., 1994; Ward et al., 1995; Venis et al., 1996;Claussen et al., 1997; Barbier-Brygoo et al., 1999

Ethylene-mediated responses Berry et al., 1996

Cold-shock responses Knight et al., 1996; Lewis et al., 1997

Nod- and pathogen-induced responses Ward et al., 1995; Zimmermann et al., 1997; Blumwald et al., 1998

Pollination Holdaway-Clarke et al., 1997; Brownlee et al., 1999

Water and solute transport Johansson et al., 1996, 1998; Logan et al., 1997; Eckert et al., 1999

Salt tolerance and turgor regulation Katsuhara and Tazawa, 1992; Taylor et al., 1996; Liu and Luan, 1998; Teodoro et al., 1998;Brownlee et al., 1999

Cellular pH regulation Johannes et al., 1998

Proton pump regulation De Boer, 1997; Claussen et al., 1997; Logan et al., 1997

450 Krol and TrebaczÐIon Channel Gating in Plant Cells

second messenger binding (Ca2�, IP3 , cGMP, cAMP). Agrowing body of evidence indicates that G-proteins, secondmessengers and phosphorylation/dephosphorylation pro-cesses mediate various plant responses through ion channeland other transport system regulation (Table 1).

Moreover, plant transmembrane receptors resemblingreceptor kinases of animal cells are involved in mediating avariety of cellular processes and responses to diverseextracellular signals (Braun and Walker, 1996; Trewavasand Malho, 1997). PCR, advanced homology-based clon-ing and function-complementation techniques have alreadyled to identi®cation of more than 70 plant protein kinasegenes (Stone and Walker, 1995). However, the precisefunction of speci®c protein kinases and phosphatasesduring plant growth and development has been elucidated
in only a few cases (Stone and Walker, 1995).
sensitivity of voltage-gated K� channels.

POTASSIUM CHANNELS

Ion transport across all biological membranes is highlyselective and thus electrochemical potentials can begenerated. The electrochemical potentials largely dependon the potassium ion gradient, so most of the potassiumchannels must remain active for long periods of time. Suchgradients are indispensable for long-term cell functionssuch as nutrition, elongation, turgor and water regulation
or osmotically driven movements (Schroeder et al., 1984;
Schroeder, 1989; Roberts and Tester, 1995; Hedrich andDietrich, 1996; Logan et al., 1997; Maathuis et al., 1997;

Ligand-gated potassium channels

Ligand binding causes conformational changes inchannel proteins. It is a process of great importance,especially during signal transduction cascades when secondmessengers synchronize the metabolism of the cell withenvironmental conditions and enhance the input stimuli.There are many K� channels a�ected by calcium ionbinding (namely: plasmalemma K�out channels, KORC,NORC, VK, FV, SVÐfor more information see below) inplant cells (Katsuhara and Tazawa, 1992; Allen andSanders, 1996; Czempinski et al., 1997, 1999; Maathuiset al., 1997; Muir et al., 1997; Allen et al., 1998a). BesidesCa2�, H� ions, nucleotides, proteins and plant hormonescan serve as potassium channel ligands (see below). Theirattachment corresponds accordingly to changes in voltage

Voltage-gated potassium channels in the plasmalemma

Voltage-gated plasmalemma K� channels are generallydivided into inward �K�� and outward (K� ) recti®ers. K�
in out in
channels are activated by hyperpolarizing potentials while

a

K�out are activated by membrane depolarization. Both K�inand K�out channels serve as membrane safeguards prevent-ing membrane voltage from becoming too negative orpositive, respectively. Such a role of voltage-gated K�channels in stabilizing membrane voltages is universalamong all eukaryotes (Maathuis et al., 1997). Voltage-dependent plasma membrane-bound outward potassiumrecti®ers responsible for K� e�ux are involved in turgorregulation (Liu and Luan, 1998), stomatal closure(MacRobbie, 1997; Grabov and Blatt, 1998a), organmovements (Iijima and Hagiwara, 1987; Stoeckel andTakeda, 1993), cation release into xylem (Roberts andTester, 1995), light-induced potential changes of theplasmalemma (Blom-Zandstra et al., 1997) or repolariza-tion during action potentials (APs), and prevention ofexcessive depolarization (Stoeckel and Takeda, 1993;Trebacz et al., 1994; Maathuis et al., 1997). These rolesare summarized in Table 2. K�in channels are involved in:potassium uptake into a cell during cell expansion, growthprocesses, organ movements and stomatal openings; low-a�nity uptake pathway in root hair cells; xylem unloadingby conducting cations from xylem to symplast of growingshoots; membrane voltage prevention against excessivehyperpolarization (reviewed by Maathuis et al., 1997)

Krol and TrebaczÐIon Ch

(summarized in Table 2).

Regulation of plasmalemma voltage-gated potassiumchannels

In addition to membrane potential, e�ectors like H�,Ca2�, nucleotides and K� ions can either interact directly(ligand binding) with both inward and outward plasma-lemma K� channels or act indirectly via membrane-bound,attached or soluble regulators (Hedrich and Dietrich, 1996;Kurosaki, 1997; Blatt, 1999; Czempinski et al., 1999).Inwardly and outwardly rectifying K� channels are con-trolled by cytosolic calcium, ATP and pH in very di�erentways (Grabov and Blatt, 1997). The action of pHcyt is mostpronounced on the depolarization-activated outward-rectifying K� channels which are virtually insensitive toincreased [Ca2�]cyt (Grabov and Blatt, 1997). They do notshow such pronounced sensitivity towards external pH butrequire slightly alkaline cytosolic pH for activation (Blattand Grabov, 1997a). Alkaline pHcyt activates IKout in avoltage-dependent manner through a co-operative bindingof two protons (Grabov and Blatt, 1997). Moreover,their activation by depolarization depends critically onphosphorylation (e.g. by a kinase tightly associated with thechannel protein in Samanea saman motor cellsÐMoran,1996) or dephosphorylation events associated with [Ca2�]cytincrease (e.g. by calcium-dependent phosphatase in Arabi-dopsis thaliana guard cellsÐMacRobbie, 1997). In meso-phyll and guard cells of Vicia faba there are outward-rectifying K� channels regulated by calcium and G-proteininteraction as well (Li and Assmann, 1993). On the otherhand, there are potential Ca2�-binding sites (EF-handmotifs) found at the C-terminus of a-subunits from putativeoutward potassium recti®ers. These ion channels are verylikely to be directly regulated by Ca2� (Czempinski et al.,
1997, 1999). This also applies to KORC and NORC
channels which become active at depolarized membranepotentials, but their respective activation depends on thecytoplasmic Ca2� level (De Boer and Wegner, 1997).KORC, NORC and SKOR are di�erent channels fromplasmalemma of root xylem parenchyma cells. They areresponsible for xylem loading (Roberts and Tester, 1995;De Boer and Wegner, 1997; Maathuis et al., 1997; Gaymardet al., 1998). KORC channels also show a considerableconductance for Na� but very low permeability for Li� andCs�. This indicates that KORC channels may also act as a`®lter' protecting the shoot from harmful Cs� or Li� ions(Maathuis et al., 1997). NORC channels discriminate onlyslightly between cations and their role in solute release intoxylem is limited. However, they do provide a function inresetting the membrane potential after excessive depolariza-tion (Maathuis et al., 1997). Kout currents conducted bySKOR are e�ectively inhibited by both cytosolic andexternal acidi®cation (Lacombe et al., 2000). SKORchannels have no Ca2�-binding sites, but they containankyrin and cyclic nucleotide-binding domains (Gaymardet al., 1998). Direct binding of nucleotides, calcium ions(De Boer and Wegner, 1997; Czempinski et al., 1997, 1999)or protons (Blatt and Grabov, 1997a) to the channelproteins illustrates that voltage-gated outward-rectifyingplasmalemma potassium channels may be regarded asligand-gated in certain experimental conditions.

Recently Ca2�-gated outward rectifying potassiumchannels have been described in the plasmalemma of thealga Eremosphaera viridis (SchoÈ nknecht et al., 1998). Thesechannels show very steep Ca2�-dependence and they can beCa2�-stimulated both directly and indirectly by interactionwith calmodulin (SchoÈ nknecht et al., 1998). They areinvolved in hyperpolarizing currents during darkening-induced transient hyperpolarizations of the plasmamembrane (Table 2).

The gating of K�out current is e�ected by [K�]ext , so thatits voltage dependence shifts in parallel with EK (Blatt,1999). K� ions bind in a co-operative fashion to a set ofsites exposed on the extracellular face of the membrane toinactivate K�out channels and they may be substituted withRb� or Cs� (Blatt, 1999). This inactivating binding ofmonovalent ions to the channel protein is facilitated byinside negative membrane voltage. Recent studies haveshown that IKout activation is also dependent on thecooperative interaction of two K� ions with the channel,but at sites di�erent from the channel pore (Grabov andBlatt, 1998a).

Voltage-dependent plant plasmalemma K�-uptake-channels represent various types (KAT, AKT) of di�erentspatial expression patterns (Bei and Luan, 1998), di�erentfunctions (Bei and Luan, 1998; Tang et al., 1998) anddi�erent sensitivities to voltage, Cs�, Ca2� and H� (Dreyeret al., 1997; Bei and Luan, 1998). This diversity partlyresults from nonselective heteromerization of di�erenta-subunits (Dreyer et al., 1997) as well as from the abilityof b-subunits to associate with more than one type ofa-subunit in vivo (Tang et al., 1996, 1998). All voltage-dependent plant plasmalemma K�-uptake-channels con-tain a conserved GYGD motif within a pore region, which

nnel Gating in Plant Cells 451

is responsible for K� conductivity (Czempinski et al.,

TABLE2.Plasm

alemmaionchannels

Channel

Permeability

Gatingmechanism

Physiologicalrole

References

Potassium

channels

K� outfrom

Vicia

fabaguard

cell

K�

Depolarization-dependentopening

Up-regulatedbypH

inincrease

(strong

voltage-dependentstim

ulation)

Co-operativebindingoftw

oprotons

K�gradientsensitive

Inhibited

byexternalK� -binding

RegulatedbyG-protein-inducedCa2� -increase

Stomatalclosure

Preventionfrom

re¯uxofK�into

theguard

cell

LiandAssmann,1993;Blattand

Grabov,1997a;Maathuiset

al.,1997;

MacRobbie,1997;Grabovand

Blatt,1998a;Leckie

etal.,1998;

Pei

etal.,1998;Blatt,1999

K� outfrom

Arabidopsisthaliana

guard

cells

K�

Depolarization-dependentopeningstim

ulated

byCa-dependentphosphatase

Up-regulatedbypH

inincrease

Stomatalclosure

MacRobbie,1997

K� outfrom

Samanea

saman

motorcells

K�Rb�Na�

Cs�

Li�

Depolarization-inducedactivation

Phosphorylationbyakinase

tightlyassociated

withK� o

utchannel

Leafmovements

Invo

lvem

entin

circadianclock

Moran,1996;Maathuiset

al.,1997

K� outfrom

Mim

osa

pudica

motorcells

K�

Activationbydepolarization

Rapid

movements

inMim

osa

RepolarizationduringAP

Stoeckel

andTakeda,1993

K� outfrom

Dionaea

muscipula

trap-lobecells

K�

Voltage-dependence

(depolarizationactivated)

Outw

ard

recti®cationstrongly

dependsonthe

concentrationofintracellularK�

Closure

oftrap-lobes

IijimaandHagiwara,1987

K� outfrom

Conocephalum

conicum

K�

Voltage-dependence

(depolarizationactivated)

RepolarizationduringAP

Trebaczet

al.,1994

KORC

(K�outw

ard

rectifying

conductance)

K�Na�

Activated

atmem

branevo

ltages

more

positive

thanÿ5

0mV

Ca2� -dependentactivation

Xylem

loading

Shootprotectionfrom

harm

ful

Cs�

andLi�

ions

Roberts

andTester,1995;DeBoer

and

Wegner,1997;Maathiuset

al.,1997

SKOR

(Shaker-typeK�outw

ard

rectifyingchannel)

K�

Voltage-dependent

Changes

inboth

pH

cytandpH

extregulate

the

number

ofchannelsavailable

foractivation

Xylem

loading

Gaymard

etal.,1998;

Lacombeet

al.,2000

NORC

(non-selective

outw

ard

rectifyingconductance)

Non-selective

amongcations

Activeat

mem

branevo

ltages

more

positive

than�3

0mV

Ca2� -dependentactivation

Protectionagainst

high

depolarization

Xylem

loading

Roberts

andTester,1995;DeBoer

and

Wegner,1997;Maathiuset

al.,1997;

White,

1998

Maxicationchannel

from

ryeroots

Non-selective

amongcations

Activeat

mem

branevo

ltages

more

positive

thanEK

Mem

branevo

ltagestabilization

White,

1998

K� outfrom

Nitellopsisobtusa

K�Na�

Ligand-binding:ATP-and[Ca2� ]

ext-dependent

regulation(inhibition)

Saltstress

tolerance

Katsuhara

etal.,1990;Katsuhara

and

Tazawa,1992

K� outfrom

Eremosphaeraviridis

K�

Ca-dependentandstim

ulatedboth

bydirect

Ca2� -bindingandindirectlybysome

calm

odulininteractions

Dark-inducedhyperpolarization

ofV

mandtherebydivalent

cationuptake

Scho Ènknechtet

al.,1998

K� outfrom

Nicotianatabacum

L.mesophyllcells

K�

Light-activation

Voltage-dependence

Mem

branedepolarizationupon

lighttransition

Blom-Zandstra

etal.,1997

K� outfrom

guard

cellsof

Vicia

fabaL.

K�

Stretch-activated

Volumeandturgorregulationand

therebycontrolofleaf

gasexchange

Cosgrove

andHedrich,1991


K� in(K

AT1)from

Vicia

faba

guard

cell

K�

Hyperpolarization-dependentopening

LoweringpH

extpromotesK�currentin

voltage-

dependentmanner

CDPK

dependentphosphorylationofKAT1

protein

inaCa2�dependentmanner

Inhibited

byIP

3-induced[Ca2� ]

inelevation

Inhibited

bypolymerized

actin®laments

Modulatedbyauxin

Controlled

byactin®laments

RequireexternalK�ionsforactivation

ModulatedbycA

MP-dependentsignallingsystem

and/ordirectcyclic

nucleotidebinding

Stomataopening

Regulationofstomatalaperture

Osm

oticvo

lumereadjustment

Blatt

etal.,1990;Fairley-G

renot

andAssmann,1992;Blatt

andThiel,

1994;WuandAssmann,1995;

Ilanet

al.,1996;BlattandGrabov,

1997a;Claussen

etal.,1997;Grabovand

Blatt,1997,1998a;Hwanget

al.,1997;

Maathuiset

al.,1997;MacRobbie,1997;

McA

insh

etal.,1997;Leckieet

al.,1998;

Liet

al.,1998;Liu

andLuan,1998;

Pei

etal.,1998;Blatt,1999;

Czempinskiet

al.,1999;Jinand

Wu,1999

KAT1from

Arabidopsisthaliana

andKST1from

guard

cellsand

¯owersofSolanum

tuberosum

K� ,

NH� 4,Rb� ,

Na� ,

Li�

Voltagedependent(hyperpolarizationactivated)

ATPandcG

MPactivation

Ionpermeationmay

feed

backongating

Competitivelyinhibited

byCa2�andCs�

ions

pH

regulated(pH

extacidi®cationshifts

voltage-dependence

toward

less

negativevo

ltages)

Regulationbycytoskeletalproteins

Modulatedbycyclic

nucleotidebinding

Stomatalopening

K�uptakeduringother

osm

otic

movements

Arm

stronget

al.,1995;Mu Èller-R

o Èber

etal.,1995;Becker

etal.,1996;Hedrich

andDietrich,1996;Hoth

etal.,1997;

Maathuiset

al.,1997;

Czempinskiet

al.,1999

AKT1from

Arabidopsisthaliana,

SKT1Ð

Solanum

tuberosum

root

cellsandchannel

analogue

from

corn

roots

K� ,

Rb� ,

Na� ,

Cs�,Li�


Inward

K�gradientsensitive

Regulationofmem

branevo

ltage

Low-a�nityK�uptake

Hedrich

andDietrich,1996;

Bertlet

al.,

1997;Maathuiset

al.,1997;

Czempinskiet

al.,1999

KIR

C(K�inward

rectifying

conductance)

K� ,

Rb� ,

Na� ,

Cs�,Li�

Activeat

mem

branevo

ltages

more

negative

thanÿ1

10mV

Xylem

unloading

Maathiuset

al.,1997

VIC

(voltage-insensitive

cation

channel)

NH� 4,Rb� ,

K� ,

Cs�,Na� ,

Li�,

TEA�

Open

60±80%

ofthetimeat

voltages

more

positive

thanÿ1

20mV

Inhibited

bydivalentcations

Low-a�nityNH� 4-uptake

Osm

oticadjustmentindependentof

themem

branepotentials

Compensatory

cation¯uxes

White,

1997,1999

K� infrom

Zea

mayscoleoptile

K� ,

Rb�


LoweringpH

ext

Inhibited

byCa2�

Modulatedbyauxin

Cellelongation

Hedrich

andDietrich,1996;

Thielet

al.,1996;Claussen

etal.,1997

K� infrom

Avenasativa

mesophyll

cells

K�

Voltage-dependent

Plasm

alemmaV

mstabilization

Stabilizationofionic

andosm

otic

conditionsduringcellexpansion

Kourie,

1996

K� infrom

Samanea

samanmotor

cells

K�

ActivationbyH�pump-inducedhyperpolarization

InhibitionbyPLC-m

ediatedIP

3-induced

Ca2�increase

Directresponse

tolight

Leafmovements

Kim

etal.,1992,1996;

Maathuiset

al.,1997

K� infrom

culturedcarrotcells

K�

Controlled

bycytoplasm

icconcentrationofcA

MP

Mem

branechanges

andthusactivation

ofvo

ltage-gated

channels

Kurosaki,1997

Stretch

activated

K� infrom

Vicia

fabaguard

cells

K�

Osm

oticum

gradient-sensitive

Voltage-dependence

Regulatedbyactin®laments

Osm

oregulation

Ramahaleoet

al.,1996;Liu

and

Luan,1998

Table

2continued

onnextpage

Krol and TrebaczÐIon Channel Gating in Plant Cells 453

TABLE2.Continued

Channel

Permeability

Gatingmechanism

Physiologicalrole

References

Calcium

channels

VDCCÐ

voltage-dependent

Ca-channel

from

guard

cells

Ca2�

Depolarizationactivated

Earlyevents

ofplanthorm

one-induced

responses

McA

insh

etal.,1995;Grabovand

Blatt,1998b

VDCC

from

ryeroots

VDCC

from

wheatroots

(rca

channel)

Ba2� ,

Sr2� ,

Ca2� ,

Mg2� ,

Mn2� ,

K� ,

Na� ,

Rb� ,

Li�


Strongvo

ltage-dependence

(depolarization

activated)

CytosolicATPshifts

activationto

more

negative

potentials

Divalentcationuptakeinto

roots

Signallingmechanismsandpriming

thecellforresponse

White,

1998;PinerosandTester,1997;

White,

1998

VDCC

from

Arabidopsisroots

andDaucuscarota

suspension

protoplasts

Ba2� ,

Sr2� ,

Ca2� ,

Mg2� ,

K�


Activeunder

conditionofmicrotubule

disorganization

Slow

inactivationat

negativevo

ltages

Cationuptake

Maintainingappropriateelectrochem

ical

gradients

importantforthetransport

ofother

ionsandcellvo

lume

regulation

Signallingmechanismsandpriming

thecellforresponse

Thionet

al.,1996;Whiteet

al.,1998

VDCC

from

characeancells

Ca2�


APinduction

Earlyevents

ofturgorregulationand

salttolerance

Katsuhara

andTazawa,1992;

Shim

men,1997

VDCC

from

Chara

corallina

Ca2�


DuringCa-starvationchannelsmight

open

toscavengeavailable

Ca2�

Reidet

al.,1997

Voltage-dependentCa-channels

from

liverwort

Conocephalum

conicum

andmoss

Physcomitrellapatens

Ca2�


Light-inducedmem

branedepolarization

Trebaczet

al.,1994;Erm

olayevaet

al.,

1996,1997

Ca-channelsfrom

mosses

Ca2�

Cytokinin-induceddepolarizationactivated

Earlyevents

ofcytokinin-induced

responses

Schumaker

andGizinski,1993

VDCC

from

Mim

osa

pudica

motorcells

Ca2�

Hyperpolarization-activated

Activationofchannelsinvo

lved

inleaf

movements

Stoeckel

andTakeda,1995

VDCC

from

pollen

tubes

Ca2�

Voltage-dependent

Stretch-activated

Growth

processes

Holdaw

ay-C

larkeet

al.,1997

VDCC

from

Fucusrhizoids

Ca2�

Voltage-dependent

Stretch-activated

Growth

processes

Tayloret

al.,1996

SAC

from

Fucuszygotes

Non-selective

Stretch-activated

Mechanosensitive

Ca-channels

from

rootcells

Non-selective

Stretch-activated

Regulatedbycytoskeletalproteins

Regulationofturgor

Determinationoftheallometry

ofcell

expansionandmorphogenesis

Thionet

al.,1996;Whiteet

al.,1998

Mechanosensitive

Ca-channels

from

guard

cells

Ca2�

Stretch-activated

Regulatedbycytoskeletalproteins

Transm

issionofCa-signalsinto

thecytoplasm

Guard

cellvo

lumeandturgorregulation

andtherebycontrolofleaf

gas

exchange

Controlofother

ionchannelswith

Ca-dependentactivities

Cosgrove

andHedrich,1991;

MacRobbie,1997;McA

insh

etal.,1997


Mechanosensitive

Ca-channels

from

Fucusrhizoids

Ca2�

Stretch-activated

Regulatedbycytoskeletonproteins

Transm

issionofCa-signalsinto

thecytoplasm

Cellvo

lumeregulation

Tayloret

al.,1996;McA

insh

etal.,1997

Receptor-regulatedCa-channels

from

parsleyprotoplastsand

rootcells

Non-selective

Elicitor-activated

Earlyevents

ofpathogen

defence

system

activation

Zim

mermannet

al.,1997;

Whiteet

al.,1998

Receptor-regulatedCa-channels

Ca2�

Elicitor-activated

Voltage-gated

Earlyevents

ofpathogen

defence

system

activation

Blumwald

etal.,1998

Receptor-regulatedCa-from

tomatoprotoplasts

Ca2� ,

K�

Elicitor-activated

Hyperpolarization-activated

Ca-in¯uxasanearlyresponse

tovarious

signalsincludingfungalelicitors

GelliandBlumwald,1997

Anionchannels

GCAC1from

Vicia

fabaand

Commelinacommunis

Clÿ,malate

S-typeshowsweakvo

ltagedependence

S-typerequires

hydrolysable

ATPandactivationof

protein

kinase

OA-sensitive

phosphatasesare

invo

lved

indown-regulationofS-typechannel

S-typemay

beABCprotein

oritistightlycontrolled

bysuch

protein

R-typeisactivated

byparallel

voltagemem

brane

depolarization,pH

cytacidi®cation,[Ca2� ]

cyt

increase

andnucleotidebinding

Directauxin

bindingshifts

activationpotential

towardsrestingpotentialsto

favo

urchannel

opening

S-typeserves

asmajorpathway

for

anione�

uxduringstomatalclosure

andasnegativefeedbackduring

stomatalopening

R-typeresponsible

forsignal

transductionvia

mem

brane

depolarization

GCAC

channelsare

capable

ofsensing

changes

intheenergystatus,acid

metabolism

andprotonpumpactivity

inguard

cells,because

oftime-

and

voltagedependentactivitystrongly

modulatedbyATPandH�

Kelleret

al.,1989;Marten

etal.,1991;

Hedrich

andJeromin,1992;

Linder

andRaschke,

1992;

Schroeder

andKeller,1992;

Schroeder

etal.,1993;Dietrichand

Hedrich,1994;

Schmidtet

al.,1995;

Ward

etal.,1995;LiandAssmann,1996;

Esser

etal.,1997;MoriandMuto,1997;

Pei

etal.,1997,1998;Grabovand

Blatt,1998a;Schwarz

and

Schroeder,1998;Leonhardtet

al.,1999

GCAC1from

Nicotiana

benthamianaandArabidopsis

thaliana

S-typeshowsweakvo

ltagedependence,requires

protein

phosphatase

activitiesandisdown-

regulatedbyprotein

kinase

S-typeisin¯uencedbypH

gradient

R-typeisactivated

byparallel

voltagemem

brane

depolarization,pH

cytacidi®cation,[Ca2� ]

cyt

increase

andnucleotidebinding

R-typeismodulatedbyphosphorylation/

dephosphorylationprocesses

Arm

stronget

al.,1995;Ward

etal.,1995;

Schulz-Lessdorfet

al.,1996;Elzengaand

VanVolkenburgh,1997b;

Lew

iset

al.,1997;Grabovand

Blatt,1998a;Pei

etal.,1997,1998

TSACÐ

tobacco

suspension-cell

anionchannel

Clÿ

ATP-controlled

voltage-dependence

(depolarization

activated)

Modulatedbyauxin

Anionrelease

duringinhibitionof

cellelongation

Zim

mermannet

al.,1994

Anionchannelsfrom

mesophyll

cellsofPisum

sativum

Clÿ

Voltage-dependent(hyperpolarizationactivated)

Twomodekineticsdi�erentlycontrolled

byATP

(R-andS-type,

S-typeoccurs

inthepresence

ofATP)

Ca-dependentactivation

Light-inducedtransientdepolarization

ElzengaandVanVolkenburgh,1997a,b

Anionchannelsfrom

suspension-

culturedcarrotcells

Clÿ


Voltage-dependentinactivationunder

large

hyperpolarization

Controlofmem

branepotential

Regulationofosm

oticbalance

Barbara

etal.,1994

Table

2continued

onnextpage


TABLE2.Continued

Channel

Permeability

Gatingmechanism

Physiologicalrole

References

Anionchannelsfrom

Eremosphaeraviridis

Clÿ

Hyperpolarizationactivated

Lim

itingtheamplitudeofdark-induced

transienthyperpolarizationcausedby

K� -release

Scho Ènknechtet

al.,1998

Anionchannelsfrom

Charophyta

cells

Clÿ


DepolarizingcurrentduringAP

Okihara

etal.,1991;Katsuhara

and

Tazawa,1992;Thielet

al.,1993;

Shim

men,1997

Anionchannelsfrom

liverw

ort

C.conicum

Trebaczet

al.,1994

Anionchannelsfrom

Aldrovanda

vesiculosa

IijimaandSibaoka,1985

Anionchannelsfrom

Physcomitrellapatens

Clÿ


Phytochrome-mediatedsignalling

pathway

Erm

olayevaet

al.,1996,1997

Anionchannelsfrom

Charophyta

cells

Clÿ

H� -

andCa2� -dependentactivation(directbinding)

Phosphorylation/dephosphorylationprocesses

Facilitationofenhancedprotone�

ux

under

intracellularacidosis

Johannes

etal.,1998

Anionchannelsfrom

epidermal

cellsofArabidopsishypocotyls

Clÿ

Strongandweakvo

ltage-dependence

ofR-and

S-typeunitary

conductances,respectively

(activationbyV

mdepolarization)

R-andS-types

havethesameconductance

but

di�erentopen

probabilities

Thesw

itch

betweenR-andS-typeiscontrolled

by

ATP(R

-typeoccurs

inthepresence

ofATP)

Modulatedbyphosphorylation/dephosphorylation

processes

R-typemay

beinvo

lved

inthe

transductionofexternalsignalsand

transm

issionofAP

S-typemay

beinvo

lved

inturgor

regulationandhypocotylmovements

Thomineet

al.,1995,1997;Choand

Spalding,1996;ElzengaandVan

Volkenburgh,1997b;Lew

iset

al.,1997;

Parkset

al.,1998

Anionchannelsfrom

epidermal

cellsofArabidopsishypocotyls

Clÿ

BL-activation(increase

inopen

probability)

Light-inducedinhibitionofcell

elongation

ChoandSpalding,1996

Anionchannelsfrom

mesophyll

cellsofPisum

sativum

Clÿ

Light-inducedactivation(increase

inopen

probability)


Light-inducedtransientmem

brane

potentialdepolarization

Chargebalance

forlight-inducedH�

pumpactivation,thuscontrolof

pH

ext,mem

branevo

ltageandosm

otic

potential

Elzengaet

al.,1995,1997;Elzengaand

VanVolkenburgh,1997a,b

SAC

from

guard

cellsof

Vicia

fabaL.

Non-selective

Stretch-activated

Reductionofcellturgor

Activationofvo

ltage-dependention

channelsthroughmem

brane

depolarization

Cosgrove

andHedrich,1991

SAC

from

Arabidopsisthaliana

guard

cells

Controlofleaf

gasexchange

Teodoro

etal.,1998


1994) (Table 2).

a

1999). Kourie (1996) demonstrated that the relative numberof opened voltage-activated inward rectifying potassiumchannels increased sigmoidally as a function of hyper-polarized membrane potential. The kinetics of inwardrectifying K� currents in Avena sativa mesophyll cellsreported by Kourie was independent of [K�]ext and it lackedtime-dependent inactivation. Neither low [K�]ext nor[Na�]ext caused inactivation of the above-mentionedcurrents, while Cs�-induced block was reversible andstrongly voltage-dependent. A role of preventing largemembrane hyperpolarization resulting from electrogenicproton pumping was proposed for these K�in channels byKourie (1996). On the other hand, there are reportsconcerning K�in channels (AKT1) `sensing' external potas-sium concentration (Bertl et al., 1997). AKT1 channels arepresent in root cells. Extracellular K� binds to a modulatorsite thereby enhancing the rate of opening of AKT1 protein.Blatt (1999) also noticed that IKin current in guard cellsrequires external millimolar K� concentrations for itsactivity. In submillimolar [K�]ext , K

�in channels appear to

enter a long-lived inactive state (Blatt, 1999).Control of plasmalemma K�in channels is modulated by

increasing [Ca2�]cyt (inactivation) and increasing externalproton concentration (voltage-dependent activation) ordecreasing pHcyt (voltage-independent activation; increasein the pool of active channels through allosteric interaction)(Ilan et al., 1996; Grabov and Blatt, 1997, 1998a; Hothet al., 1997; MacRobbie, 1997). Ca2�-dependent inactiva-tion can proceed even when pH is bu�ered. Equally,changes in pH and channel gating may occur withoutmeasurable changes in calcium concentration (Allan et al.,1994; Armstrong et al., 1995). Thus, the e�ects of cellularpH and calcium are separable, although these two ionicmessengers do interact. In other words, pHcyt may act inparallel with, but independently of, [Ca2�]cyt in controllingK�in channels (Grabov and Blatt, 1997). Kim et al. (1996)reported that phosphoinositide turnover, phospholipase C(PLC) activation or the presence of inositol triphosphate(IP3) is correlated with K�in channel closure. Earlier, Blattet al. (1990) demonstrated the possibility of controlling K�inchannel activity by IP3-mediated Ca2� release. Both theabove-mentioned results indicate that increase in [Ca2�]cyt isresponsible for K�in channel inactivation and they support agrowing body of evidence that G-proteins function inregulating IKin (reviewed by Blatt and Grabov, 1997a,b).Recently, Li et al. (1998) identi®ed a Ca2�-dependentprotein kinase, with a calmodulin-like domain (CDPK),which phosphorylates K�in channels of Vicia faba guard cellprotoplasts. Moreover, the cAMP-dependent signallingsystem `cross-talks' with Ca2�-dependent inhibition of K�inchannels from Vicia faba guard cells by reversing inhibitorycalcium e�ects (Jin and Wu, 1999). In contrast to K�inchannels from guard cells, K�in channels in the plasma-lemma of rye root cells are insensitive to [Ca2�]cyt (White,1997).

K�in channels (KAT1ÐArabidopsis thaliana, KST1ÐSolanum tuberosum) can also be inhibited by Ca2� and Cs�via competition in binding to the pore forming regionexposed to the aqueous lumen of the channel (Becker et al.,


1996). Thiel et al. (1996) showed that Ca2�-binding to the

K� channel protein is responsible for fast and reversibleinactivation of inward K� currents in maize coleoptileprotoplasts.

In addition to their Ca2� and pH dependence, voltage-gated plasmalemma K�in channels seem also to require ATP(Hoshi, 1995; MuÈ ller-RoÈ ber et al., 1995; Wu and Assmann,1995). Their structures contain ATP and cyclic nucleotide-binding cassettes in the C-terminal domains. The rundownof K�in recti®ers in the absence of ATP is explained in termsof a shift in the voltage-dependence (Hedrich and Dietrich,1996). Kurosaki (1997) surveyed some of the inward K�channels (located in the plasma membrane of culturedcarrot cells) whose gating was controlled by cytoplasmicconcentration of cAMP. Their activation resulted intransient membrane potential changes, which in turnactivated voltage-gated Ca2� channels. Because plasma-lemma voltage-gated inward K�-channels described byHedrich and Dietrich (1996) and Kurosaki (1997) areregulated via direct nucleotide binding to the channelprotein, they can be classi®ed as ligand-gated ones as well.

There is an obvious correlation between inward rectifyingK� channels and cytoskeletal proteins (Table 2). As aconserved structural feature, proteins of the AKT subfamilycontain so-called ankyrin repeats which are potentialdomains for interaction with the cytoskeleton (Czempinskiet al., 1999). Because proteins from the KAT subfamily lacksuch ankyrin sequences, but they are `sensitive' tocytoskeletal drugs, there must be other channel domainsparticipating in the regulation by cytoskeletal compounds(Hwang et al., 1997; Czempinski et al., 1999). Pharmaco-logical studies on guard cells have shown that actin®laments contribute to regulation of K�in channels as wellas of stomatal aperture (Hwang et al., 1997). CytochalasinD, which induces depolymerization of actin ®laments,activates inward potassium currents, while phalloidinÐastabilizer of ®lamentous actinÐinhibits them (Hwang et al.,1997). These authors demonstrated that polymerized actinstabilizes K�in channels in the closed state and thus makesthem unresponsive to membrane hyperpolarization. Asactin ®laments depolymerize, the closed state of K�inchannels becomes less stable and more channels becomeready to respond to the hyperpolarized membrane poten-tial. Liu and Luan (1998) also correlated regulation of IKinwith the pattern of organization of actin ®laments. Theystated that actin structure may be a critical component inthe osmosensing pathway conducted by K�in channels inplants.

There are also reports of auxin-induced modulation ofK�-inward recti®ers at the plasma membrane in coleoptilecells (Claussen et al., 1997) and guard cells (Blatt and Thiel,


Voltage-gated potassium channels in the tonoplast

In the tonoplast of higher plants there are three distinctkinds of voltage-sensitive potassium channels (FV, fastactivating; SV, slow activating; and VK, strongly K� select-ive) (Table 3). FV channels are instantaneously activated atthe resting levels of [Ca2�] and pH by changes in
cyt cyttonoplast voltage (Allen et al., 1998). They open at cytosol

TABLE3.Ionchannelsin

plantendomem

branes

Channel

Permeability

Gatingmechanism

Physiologicalrole

References

Potassium

channels

Tonoplast

FV

(fast-activating)

cationchannels

NH� 4,K� ,

Rb� ,

Cs�,

Na� ,

Li�

Voltage-dependentopen

probability

Preferred

outw

ard

recti®cationat

positive

potentials

(relativeto

thecytoplasm

)Activeat

therestinglevelsof[Ca2� ]

cytandpH

cyt

Inhibited

byvacuolarandcytosolicCa-increases

FV

currents

are

reducedat

acidic

pH

cyt

ATPregulated

Blocked

byMg2�andpolyamines

Controlofthetonoplast

electrical

potentialdi�erence

aroundEK

Ashuntconductance

forthe

vacuolarH�pumps

Invo

lvem

entin

potassium

release

duringstomatalclosure

Invo

lvem

entin

increase

incellular

osm

olarity

Smallmonovalentcationuptake

LinzandKo Èhler,1994;Allen

andSanders,

1996,1997;Maathuiset

al.,1997;

Tikhonovaet

al.,1997;Allen

etal.,1998a;

GrabovandBlatt,1998a;B

ruÈggem

annetal.,

1999a,b;Dobrovinskayaet

al.,1999

Tonoplast

SV

(slow-activating)

cationchannels

K� ,

Na� ,

Rb� ,

Li�,

NH� 4,Ca2� ,

Mg2� ,

polyamines

Tim

e-dependentactivationat

cytosol-positive

potentials

Outw

ard-rectifying

Strongvo

ltage-dependence

modulatedbyCa2� ,

Mg2�

andH�ions(C

a-andMg-activationanddown-

regulationofSV

channel

activitybyprotons)

Ca2�inducesloweringofthevo

ltagethreshold

for

activation

RequirealkalinepH

atboth

sides

oftonoplast

Regulatedbyprotein

phosphorylationandcalm

odulin

interaction

Single

channel

conductance

dependenton[K� ]

cyt

Modulatedbyredoxagents

(increasedopen

probability

inthepresence

ofantioxidants)

Blocked

bypolyamines

inavo

ltage-dependentmanner

Vacuolarreceptorsite

forcalcium

duringstomatalclosure

Possible

participationin

CIC

R(C

a-inducedCa-release)

Turgorregulation

Vacuolariontransport

Ward

andSchroeder,1994;Allen

and

Sanders,1995,1996,1997;Schulz-Lessdorf

andHedrich,1995;Ward

etal.,1995;

Gambale

etal.,1996;Bethkeand

Jones,1997;Maathuiset

al.,1997;

MacRobbie,1997;McA

insh

etal.,1997;

Allen

etal.,1998b;GrabovandBlatt,

1998a;Carpanetoet

al.,1999;Ceranaet

al.,

1999;Dobrovinskayaet

al.,1999

Tonoplast

VK

(vacuolarK� )

channels

K� ,

Rb� ,

NH� 4

Activated

bymicromolar[Ca2� ]

cytandacidic

pH

cyt

Voltage-independent,non-rectifyingchannel

Ca-dependentpotassium

uptakeand

release

duringstomatal

movements

(e.g.ABA-induced

stomatalclosure)

Activationofvo

ltage-gated

tonoplast

channels

Ward

etal.,1995;Allen

andSanders,1996,

1997;Maathuiset

al.,1997;

MacRobbie,1997;McA

insh

etal.,1997;

Allen

etal.,1998a;GrabovandBlatt,1998a

Cation-selective

channel

from

tonoplast

ofalgae

Lamprothamnium,Chara

buckellii,Chara

australisand

Nitellopsisobtusa

K� ,

Na�

Activated

bymicromolar[Ca2� ]

cyt

Voltagedependence

StrongpH-dependence

(inhibitionbyacidic

pH)

Osm

oticvo

lumeandturgor

regulation

Katsuhara

andTazawa,1992;

Lu Èhring,1999

Cation-selective

channel

from

thylakoidsofSpinacea

oleracea

andPisum

sativum

cotyledons

K� ,

Ca2� ,

Mg2�

Voltage-gated

(activated

bypositive

mem

branepotentials

ofstromarelative

tolumen)

Compensationoflight-induced

proton¯uxes

PottosinandScho Ènknecht,1996;

HinnahandWagner,1998

Cation-selective

channel

from

chloroplast

envelope

Multi-cation

Voltage-dependent

Metabolite

di�usion

Heiber

etal.,1995

Cation-selective

channel

from

chloroplast

envelope

K�

Voltage-dependent

ATP-regulated

ModulatedbyCs�,Mg2�

Compensationoflight-driven

protonmovements

Heiber

etal.,1995

Cation-selective

channel

from

nuclearenvelopefrom

redbeet

Multi-cation

Ca-regulatedvo

ltage-dependence

Ca-regulatedpathwaysfornuclear

processes

GrygorczykandGrygorczyk,1998


Calcium

channels

Ligand-gated

Ca-channel

from

vacuole

andER

ofcauli¯ower

andvacuolesofguard

cells,

zucchinihypocotyls,oat

roots,

carrotandredbeetroots,mung

beanhypocotyls,maizecells

Ca2�

ActivationbyIP

3-binding

Ca-currentrecti®cationoverphysiologicaltonoplast

potentials(cytosolnegativewithreference

tolumen)

Ca2� -release

duringsignal

transduction

MuirandSanders,1996,1997;Allen

and

Sanders,1997;Muiret

al.,1997;Leckie

etal.,1998;MacRobbie,1997;McA

insh

etal.,1997

Ligand-gated

Ca-channel

invacuolesfrom

redbeets

and

cauli¯ower

¯orets

Ca2� ,

K�

ActivationbycA

DPR-binding

Ca2� -release

duringsignal

transduction

Allen

etal.,1995;MuirandSanders,1996;

Allen

andSanders,1997;McA

insh

etal.,

1997;Muiret

al.,1997;Leckie

etal.,1998

Ligand-gated

Ca-channel

from

algaEremosphaeraviridis

Ca2�

ActivationbycA

DPR-binding

Ca2� -release

duringsignal

transduction

Bauer

etal.,1998

VVCa(voltage-gated

Ca-

channelsfrom

vacuolesofVicia

fabaguard

cellsandBeta

vulgarisroots)

Ca2� ,

K�


pH-sensitive

Requiretw

oCa2�ionsbindingto

open

LuminalCa2�shiftsthethreshold

forvo

ltageactivationto

less

negativepotentials

Inhibited

by[Ca2� ]

cytincreases

IntracellularCa2� -release

Allen

andSanders,1994,1997;Johannes

andSanders,1995;McA

insh

etal.,1997;

PinerosandTester,1997

Ca-channel

from

ER

ofBryonia

diodicatendrils

Ca2�

Voltage-dependent

Ca2� -gradientsensitive

IntracellularCa2� -release

during

responsesto

mechanicalstim

uli

KluÈsener

etal.,1995

Anionchannels

Vacuolarmalate

channelÐ

VMal

from

Arabidopsisthaliana

vacuoles

Malate

fumarate,

acetateNOÿ 3;

H2POÿ 4

Activationbypotentialsmore

negativethanEMal

Stronginward

recti®cationbecause

ofluminalClÿ

blockadeofmalate

re-entry

Vacuolarmalate

uptake

Ceranaet

al.,1995;Allen

andSanders,

1997;Che�

ngset

al.,1997

VacuolarchloridechannelÐ

VCl

Clÿ,NOÿ 3;

SO

2ÿ

4

Activationbytonoplast

hyperpolarization(negative

potentialsrelative

tothecytoplasm

)Ðinward-recti®cation

Vacuolaranionuptake

Allen

andSanders,1997

VacuolarVClfrom

Vicia

faba

guard

cells

Clÿ

Activationbytonoplast

hyperpolarization

Channel

activationdependsonprotein

phosphorylation

Inward-recti®cation

Anionuptakeduringstomatal

opening

Pei

etal.,1996;GrabovandBlatt,1998a

Vacuolaranionchannel

from

Characeancells

Clÿ,NOÿ 3

Outw

ard

rectifyingCa-dependentregulation

Turgorregulation

Katsuhara

andTazawa,1992

VDAC

(voltage-dependentanion

channelsin

outermem

braneof

mitochondria)

Non-selective

Voltage-dependent

pH-dependent

Secondmessenger-binding

Controlofmitochondrialmem

brane

potential

ControlofATPdi�usion

Controlofsignaltransduction

Elkeles

etal.,1997;Mannella

etal.,1997,

1998;RostovtsevaandColombini,1997;

Green

andReed,1998;Songet

al.,1998;

Shim

izuet

al.,1999

Inner

mem

braneanionchannel

from

mitochondria

Non-selective

pH-regulated(activated

bylow

matrixpH)

Anionuniport

BeavisandVercesi,1992

Anionchannel

from

outer

envelopeofchloroplasts

Non-selective

Voltage-dependent

Metabolite

di�usion

Heiber

etal.,1995;Pohlm

eyer

etal.,1998

Anionchannel

from

inner

envelopeofchloroplasts

Clÿ

Voltage-dependent


protonmovements

Heiber

etal.,1995;FuksandHomble,1999

Anionchannel

from

thylakoids

Clÿ

Voltage-dependent


protonmovements

Heiber

etal.,1995;Pottosinand

Scho Ènknecht,1995

9

vacuolar membrane face (LuÈ hring, 1999).

a

positive vacuolar membrane potential for longer times thanat negative potentials and hence they mainly allow K� andNH�4 e�ux from the cytoplasm into the vacuole (preferredoutward recti®cation) (Tikhonova et al., 1997; BruÈ ggemannet al., 1999b). Their function is to control the electricalpotential di�erence across the tonoplast (Tikhonova et al.,1997). Vacuolar Ca2� suppresses FV channels in a voltage-dependent manner while cytosolic Ca2� blocks them in avoltage-independent manner (Allen and Sanders, 1996;Tikhonova et al., 1997; Allen et al., 1998a). One of the mostpronounced features of FV channels is their blockade byMg2�. Increasing cytosolic free Mg2� decreases the openprobability of FV channels without a�ecting single currentamplitudes (BruÈ ggemann et al., 1999a). FV currents werealso shown to be reduced at acidic pHcyt (Linz and KoÈ hler,1994) or by cytosolic polyamines (Dobrovinskaya et al.,1999). Recent studies on FV currents in red beet vacuolesindicate that FV channels may be ATP regulated (Allenet al., 1998a).

SV channels are strictly outward rectifying, cationselective and they show characteristics typical of a multi-ion pore, i.e. more than one ion can occupy the channelpore at the same time (Allen and Sanders, 1996). Theydisplay time-dependent activation at cytosol-positive poten-tials and when [Ca2�]cyt is higher than approx. 0.5 mM(Schulz-Lessdorf and Hedrich, 1995; Allen and Sanders,1996). Calcium and protons modulate the voltage-dependence of SV channels (Schulz-Lessdorf and Hedrich,1995). These two cations interact strongly with the voltagesensor without changing the unitary conductance. Theopen probability of the SV-type channel is a function of[Ca2�]cyt (Gambale et al., 1996). Schulz-Lessdorf andHedrich (1995) showed that there is a regulatory Ca2�-binding site on the cytoplasmic face of the SV channel andthat calmodulin may be involved in the modulation of theactivation threshold of the SV-type channel. This is inagreement with recent results of Bethke and Jones (1997)who examined SV currents stimulated by both calmodulin-like domain protein kinase (CDPK) and okadaic acid-sensitive phosphatases. On the other hand, Ca2�-dependentprotein phosphatase can induce the inhibition of SVchannels (Allen and Sanders, 1995). Bethke and Jones(1997) proposed a model in which SV channel activity isregulated by protein phosphorylation at two sites. In theabsence of calcium ions, Mg2� can activate SV currents(Allen and Sanders, 1996; Cerana et al., 1999). Moreover,the single channel conductance increases as a function ofthe potassium concentration (Gambale et al., 1996). Thisbehaviour can be explained by a multi-ion occupancymechanism. However, at negative transtonoplast voltages,the closure of SV channels is una�ected by either Ca2� orMg2�, indicating that the channel belongs to the voltage-gated superfamily (Cerana et al., 1999). SV channels arealso reversibly activated by a variety of sulphydryl reducingagents at the cytoplasmic side of the vacuole (Carpanetoet al., 1999). Increase in the open probability in the presenceof antioxidants may correlate ion transport with othercrucial mechanisms that in plants control turgor regulation,response to oxidative stresses, detoxi®cation and resistance

460 Krol and TrebaczÐIon Ch

to heavy metals (Carpaneto et al., 1999).

Cytosolic polyamines are strong inhibitors of SVchannels, but in contrast to the inhibition of FV channels,the blockage of SV channels displays a pronounced voltage-dependence (Dobrovinskaya et al., 1999). Hence,polyamine-blockage is relieved at a large depolarization(because of the permeation of polyamines through thechannel pore) and in the presence of high concentrations ofpolyamines the slow vacuolar channels are converted intoinward recti®ers (Dobrovinskaya et al., 1999).

VK channels are non-rectifying and are activated atmicromolar [Ca2�]cyt and acidic pHcyt by tonoplast poten-tials ranging from ÿ100 to �60 mV (Allen and Sanders,1996; Allen et al., 1998a). Therefore, they can be involved invacuolar potassium uptake and loss. So far their presencehas been proved only in guard cells.

Di�erent sensitivities of FV-, SV- and VK-channels to[Ca2�]cyt and pH may provide a mechanism whereby stimuliactivating various signalling pathways can generatevacuolar ion uptake or loss. Muir et al. (1997) concludedthat this di�erential regulation of vacuolar channels byCa2� represents a downstream event in signal transductioncascades induced by Ca2�-release. SV channels are thoughtto participate in signalling processes because of their abilityto release Ca2� after Ca2�-dependent activation (CICRÐCa2�-induced Ca2�-release) (Allen et al., 1998b). However,Pottosin et al. (1997) demonstrated that the SV channel isnot suited for CICR from vacuoles, at least in the case ofbarley mesophyll cells. Thus, the physiological role of SVchannels remains a matter for discussion.

The most frequently observed voltage-gated K�in -channelin the tonoplast of Chara was examined by LuÈ hring (1999)(Table 3). Acidi®cation on both sides of the membranedecreases open probability of the channel and changes itsvoltage-dependence, most probably through protonation ofnegatively charged residues in neighbouring voltage-sensingtransmembrane domains (LuÈ hring, 1999). The channelbehaves like animal maxi-K channels and its gating kineticsresponds to cytosolic Ca2�. Under natural conditions,pH changes contribute mainly to channel regulation at the

nnel Gating in Plant Cells

Voltage-gated potassium channels in other intracellularmembranes

Heiber et al. (1995) showed that the chloroplast envelopecontains voltage-dependent cation channels (Table 3) withcomplex gating behaviour and subconductace states, as wellas cation-selective pores with high conductances. Voltage-dependent cation channels favour potassium uptake andtheir gating is a�ected by monovalent cations (Cs�),divalent cations (Mg2�) and millimolar concentrations ofATP. Hinnah and Wagner (1998) observed potassiumselective pore-like channels in osmotically swollen thyla-koids from pea protoplasts derived from cotyledons ofyoung Pisum sativum plants (Table 3). There is also anonselective (PK 4 PMg 4 PCa) cation channel in nativespinach thylakoid membranes (Table 3) found by Pottosinand SchoÈ nknecht (1996). This cation channel displaysbursting behaviour and its open probability increases at
positive membrane potentials (Pottosin and SchoÈ nknecht,

a

1996). It has only a moderate voltage-dependence com-pared to classical voltage-dependent recti®ers. It is postu-lated that its function is to compensate the light-drivenproton uptake into thylakoids (Pottosin and SchoÈ nknecht,1996).

A Ca2�- and voltage-dependent non-speci®c channel wasfound in the nuclear envelope of red beet (Grygorczyk andGrygorczyk, 1998) (Table 3). Micromolar [Ca2�] on thenucleoplasmic side of the envelope activates this cationchannel. The channel voltage-dependent activity changeswith the nucleoplasmic calcium concentration. Such achannel may provide a Ca2�-regulated pathway for Ca2�-


dependent nuclear processes (e.g. gene transcription).

skeletal ®bres (Sievers et al., 1996).
Plasmalemma voltage-insensitive cation channels (VIC)
The VIC channels are responsible for an in¯ux of a rangeof monovalent cations into cereal root cells (Table 2). It hasbeen postulated that they could contribute to low-a�nityNH�4 uptake and rapid osmotic adjustment independent ofmembrane potential. They may also compensate electro-genic cation ¯uxes (White, 1999). Under saline conditionsVIC channels along with K�in channels play a major role inthe toxic Na� in¯ux across the plasma membrane (White,1999). Inward currents through the VIC channels are
inhibited by Ca2� and Ba2�.
(discussed by Szarek and Trebacz, 1999).

( facilitating Ca2� in¯ux to the cytosol).

Stretch-activated potassium channels

Changes in turgor pressure induced by hyper- or hypo-osmotic stress induce an early change in activities of stretch-sensitive channels. Stretch-activated channels (SACs) alsorespond when mechanical forces are exerted on the cell(Ramahaleo et al., 1996). For the translation of membranestretch into channel gating it is generally argued thatattachment of membrane proteins to tension-transmittingcomponents is necessary, by linkage to cell wall proteins, orcytoskeletal proteins, or both (MacRobbie, 1997). Anionic,cationic, as well as non-selective SACs, have been reportedto occur in plasma membranes (Table 2). There is agrowing body of evidence for involvement of stretch-activated ion channels in regulation of the response ofguard cells to ABA through interactions with the cyto-skeleton (MacRobbie, 1997; McAinsh et al., 1997). Liu andLuan (1998) identi®ed two kinds of stretch-activatedpotassium channels in Vicia faba guard cells: voltage-gated and insensitive to membrane potential. This was the®rst evidence that plants contain osmosensitive, voltage-dependent channels, those previously described by Rama-haleo et al. (1996) being voltage-independent. Negativepressure activates voltage-insensitive currents with conduct-ance very di�erent from that of voltage-dependent K�-channels. Voltage-dependent currents (IKin and IKout) are inturn sensitive to osmotic gradient rather than changes inpressure, although actin ®laments are involved in IKinregulation (Liu and Luan, 1998). Hypotonic conditionsactivate IKin and inactivate IKout , while hypertonic con-ditions act in the opposite way. An alternation in channelopening frequency is responsible for regulating I and
KinIKout under di�erent osmotic conditions. Hypertonic
inhibition of IKin can be prevented by disruption of actin®laments. Actin ®lament disruption occurs in hypotonicconditions providing a link between hypotonic stress andhypotonic activation of the inward K� channels. Alsocytochalasin D (a cytoskeleton disrupting drug) modulatesIKin in a similar way to hypotonic conditions (Liu andLuan, 1998), which is consistent with the report of Hwanget al. (1997). It seems reasonable that stretch-activatedchannels in the plant plasma membrane, which is undercontinuous compression resulting from turgor pressure andthe presence of the cell wall, interact with cytoskeletalstructures providing local stretch of the membrane. It ispostulated that during perception of gravitational stimuli,statoliths exert local stretch on the membrane via cyto-


Light-activated potassium channels

Blom-Zandstra et al. (1997) examined light e�ects onvoltage-gated K�out channels in mesophyll protoplasts ofNicotiana tabacum (Table 2). Single channel data frompatch-clamp studies indicate that the activity of the channelincreases upon dark-light transition. The e�ect of light wasnot observed in root cells or chlorophyll-de®cient cells,suggesting that such a response requires photosyntheticactivity. These results are consistent with those of Kim et al.(1992) who showed that K� channels display responses tolight. The light activated ion channels and electrogenicproton pump are regarded as important factors in the notyet fully understood light stimulus transduction cascade

CALCIUM CHANNELS

Calcium ions are universal second messengers in plant andanimal cells. They mediate in various signalling pathways(reviewed by Brownlee et al., 1999; Sanders et al., 1999)from signal perception to gene expression, through theactivation of ion channels and enzyme cascades. Stimulus-induced increases in [Ca2�]cyt encode information as speci®cspatial and temporal changes in frequency of [Ca2�]cytoscillationsÐthe `calcium signature' (McAinsh et al.,1997; Leckie et al., 1998). After signal transition, excessCa2� must be sequestered into external and internal storesto keep [Ca2�]cyt at a low level ranging from tens tohundreds nM. Thus, all Ca2� channels located in Ca2�-sequestering membranes are strongly inward rectifying

Ligand-gated calcium channels in plasma membrane

Recently, Zimmermann et al. (1997) reported a novelCa2�-permeable, La3�-sensitive plasma membrane ionchannel of large conductance (Table 2). The channel isactivated by elicitors and is essential in pathogen defence.Receptor-mediated stimulation of these channels appears tobe involved in the signalling cascade triggering a pathogendefence system. The activation of plasma membrane Ca2�-channels by speci®c and non-speci®c elicitors provides a
direct demonstration of a pathway by which [Ca2�]cyt

(Muir et al., 1997).

a

increases to levels that can initiate the production of activeoxygen species, callose and phytoalexins via Ca2�±


dependent gene expression (Blumwald et al., 1998).

aperture changes.

Ligand-gated calcium channels in inner membranes

Ligand-gated Ca2� channels in plant cells reported todate represent two classes: IP3 (inositol triphosphate)- orcADPR (cyclic ADP-ribose)-gated (Table 3). Recently anew signalling moleculeÐNAADP (nicotinic acid adeninedinucleotide phosphate)Ðhas been found in animal cells(Lee, 2000). Ligand-gated Ca2� channels are present only inintracellular compartments, and thus their existence pro-vides a convenient mechanism for linking perception ofstimuli (e.g. light, IAA, ABA, osmotic shock, pollination,Nod-factors, cold shock) to intracellular calcium mobiliza-tion (Knight et al., 1996; McAinsh et al., 1997; Muir et al.,1997; Trewavas and Malho, 1997). The IP3-induced Ca2�-release originates mainly from vacuolar stores, although incauli¯ower, Muir and Sanders (1997) found at least twodistinct membrane populations sensitive to IP3. IP3-inducedCa2�-currents are inwardly rectifying and highly selectivefor calcium (Allen and Sanders, 1997). A speci®c IP3-binding 400-kDa protein, which is competent to releaseCa2� when incorporated into proteoliposomes (Biswaset al., 1995), was puri®ed from mung bean, though nosubsequent reports on this protein have appeared. There issome indirect evidence for the presence of IP3-gated Ca2�channels in the tonoplast of the algae Chara and Nitella(Katsuhara and Tazawa, 1992).

As well as IP3-gated channels, cADPR-gated Ca2�channels act as instantaneous strong inward recti®ers overphysiological membrane potentials and they are activatedby ligand binding only in the presence of calcium on theluminal side of the membrane. Pharmacological studiessuggest that cADPR has the capacity to act as a Ca2�-mobilizing intracellular messenger and an endogenousmodulator of Ca2�-induced Ca2� release (CICR) (Willmottet al., 1996). Ryanodine and ca�eine (agonists of ryanodinereceptors in animal cells) are able to cause activation ofcADPR-gated channels in a dose-dependent manner (Allenet al., 1995), while ruthenium red and procaine (antagonistsof ryanodine receptors in animal cells) block Ca2� release(Allen et al., 1995; Muir and Sanders, 1996; Bauer et al.,1998) in plant cells. Heparin of low molecular mass andTMB-8, well known competitive inhibitors of IP3-receptorsin plant and animal cells, are without e�ect on cADPR-gated Ca2�-channels (Muir and Sanders, 1996). Allen et al.(1995) demonstrated that there is a relatively low density ofcADPR-gated channels in beet microsomes. cADPR-gatedchannels could participate in calcium release only up to25% in comparison to the dominating IP3-induced Ca2�-release. Similar results were obtained from cauli¯owermicrosomes (Muir et al., 1997) and the unicellular greenalga Eremosphaera viridis (Bauer et al., 1998). Preliminaryexperiments on sea urchin egg homogenates indicate thatcADPR may bind to an accessory 100±140 kDa protein(Galione and Summerhill, 1996).

The lack of modulation of plant ligand-gated Ca2�-
channels by cytosolic Ca2� is the most notable di�erence
recognized to date between these and animal channels


Voltage-gated calcium channels in the plasmalemma

Many voltage-gated Ca2� channels have been describedin a variety of plant tissues and species (reviewed by Pinerosand Tester, 1997) (Table 2). Most of these are activatedthrough membrane depolarization and stimuli causingmembrane depolarization such as increased [K�]ext(Thuleau et al., 1994), Ca2� starvation (Reid et al., 1997),cytokinins (Schumaker and Gizinski, 1993), light orelectrical pulses (Trebacz et al., 1994; Ermolayeva et al.,1996, 1997) mechanical stimulation (Shimmen, 1997), ABA(McAinsh et al., 1995; Grabov and Blatt, 1998b) andmicrotubule inhibitors (Thion et al., 1996). White (1998),focusing on Ca2� channels in the plasma membrane of rootcells, distinguished between them based on their di�erentsensitivities to La3�, Gd3� and verapamil. He discussedtheir roles in mineral nutrition, intracellular signalling andpolarized growth.

Kiegle et al. (2000), Gelli and Blumwald (1997) andStoeckel and Takeda (1995) described the hyperpolariza-tion-activated in¯uxes of Ca2� through the plasmalemma.The hyperpolarization-activated calcium current is postu-lated to allow nutritive Ca2� uptake. Hyperpolarization-activated Ca2� channels described in the plasma membraneof Vicia faba guard cells by Fairley-Grenot and Assmann(1992) are in fact the inwardly rectifying K� channelsmediating Ca2� in¯ux prior to their closure and they maybe involved in the regulatory mechanism of stomatal

Voltage-gated calcium channels in inner membranes

Voltage-gated Ca2�-channels are also present in othercell compartments such as the vacuole, thylakoids or ER(Pineros and Tester, 1997) (Table 3). Vacuolar voltage-gated Ca2� channels (VVCa), characterized by Allen andSanders (1994), behave as multi-ion pores inwardly rectify-ing over the voltage range between ÿ20 and ÿ50 mV(hyperpolarization). Their activity is inhibited by lantha-nides, verapamil, nifedipine and by [Ca2�]cyt above 1 mM.Luminal Ca2� shifts the threshold for VVCa activation to aless negative potential, and therefore restricts the accumu-lation of calcium excess in the vacuole. Luminal pH ofabout 5.5 prevents uncontrolled leakage of Ca2�, because atthis physiological pH value the channel openings are veryinfrequent (the highest activation is around pH 7).Johannes and Sanders (1995) showed that a binding oftwo calcium ions is required to open the VVCa channel.Voltage-gated vacuolar Ca2� channels, previouslydescribed in tonoplasts of beet, Arabidopsis and tobacco,are in fact manifestations of SV K� channels (Ward andSchroeder, 1994).

KluÈ sener et al. (1995, 1997) have shown the voltage-gatedCa2� channels derived from endoplasmic reticulum mem-branes of Bryonia dioica touch-sensitive tendrils. The rangeof membrane potentials activating these channels was
a�ected by the Ca2� gradient across the membrane. Single

a

channel currents were modulated by divalent cations,protons and H2O2 . H2O2 is a strong inhibitor of thesechannels. The channel conductance increases with cytosolacidi®cation. These channels play an important role in themodulation of [Ca2�] in response to changes in [H O ]


cyt 2 2 cytor pH .

in turgor/volume regulation and signal transduction.

[Ca2�] is assumed to occur during turgor regulation.

cyt

Stretch-activated calcium channels

Taylor et al. (1996) examined both stretch-activated andvoltage-gated mechanosensitive Ca2�-permeable cationchannels in subprotoplasts prepared from di�erent regionsof rhizoid and thallus cells of Fucus zygotes (Table 2). Theirresults suggest that intercellular signal transduction ispatterned by interactions of the cell wall, plasma membraneand intracellular Ca2� stores.

Thion et al. (1996) observed activation of voltage-gatedCa2� channels by microtubule disruption. Their results areconsistent with a previous report of Davies (1993), whopostulated that variation potentials can be transduced viamechano-sensitive Ca2� channels into gene expressionthrough Ca2�-dependent cytoskeleton-associated phos-phorylation/dephosphorylation processes. In addition,Ca2� in¯ux through `volume sensing' voltage-gated Ca2�channels is essential for an apical Ca2� gradient to bemaintained in a growing cell (Taylor et al., 1996; Holdaway-
Clarke et al., 1997).
ANION CHANNELS

Plant anion channels regulate anion e�ux from a cellthrough plasmalemma (Table 2) and/or tonoplast(Table 3). Anion e�ux from the cytoplasm into theextracellular space is driven by the anion gradient and thenegative membrane potential causing plasma membranedepolarization, which in turn activates outward rectifyingvoltage-gated K� channels. Anion-induced depolarizationplays a crucial role in such processes as xylem loading,generation and propagation of action potentials or light-induced transient voltage changes of membrane potential.In addition, anion and potassium losses promote osmo-regulation, stomatal closure, tissue and organ movements.Since plant cells experience low extracellular anion concen-trations, anion uptake must be energetically coupled with
proton pumps.
Ligand-gated anion channels in the plasmalemma

There are many anion channels activated by cytoplasmiccalcium widespread in plant cells (Katsuhara and Tazawa,1992). Ca2�-dependent anion channels are responsible forthe main depolarizing current during action potential inCharophyta (Okihara et al., 1991; Katsuhara and Tazawa,1992; Thiel et al., 1993; Shimmen, 1997), the liverwortConocephalum conicum (Trebacz et al., 1994), Aldrovandavesiculosa (Iijima and Sibaoka, 1985) and during phyto-chrome-mediated transient depolarization in the mossPhyscomitrella patens (Ermolayeva et al., 1996, 1997).

Johannes et al. (1998) showed a direct e�ect of cyto-
plasmic protons on Clÿ e�ux in Chara corallina during
intracellular acidosis. H�-activated anion channels respon-sible for Clÿ currents act to facilitate an enhanced protone�ux under conditions of low pHcyt . Activity of thesechannels is also indirectly pH- and Ca2�-dependentthrough phosphorylation/dephosphorylation processes.The above-mentioned ®ndings imply that plasmamembrane anion channels play a central role in pHcytregulation in plants, in addition to their established roles


Ligand-gated anion channels in the tonoplast

Katsuhara and Tazawa (1992) summarized calcium-regulated channels and their bearing on physiologicalactivities in characean cells. They presented some evidencefor the presence of Ca2�-regulated anion channels in thetonoplast of Chara, Nitellopsis and Lamprothamnium giantinternodal cells (Table 3). Activation of these channels by

cyt

Voltage gated anion channels in the plasma membrane

In the plasma membrane, voltage-gated anion channelsare activated by depolarization and under an excess ofcytoplasmic Ca2�. They deactivate under hyperpolarizingpotentials (Keller et al., 1989; Hedrich et al., 1990; Hedrichand Jeromin, 1992; Linder and Raschke, 1992; Schroederand Keller, 1992; Dietrich and Hedrich, 1994; Thomineet al., 1995; Schultz-Lessdorf et al., 1996; Lewis et al., 1997;Pei et al., 1998). Inverse voltage dependence (activation byhyperpolarization) has been reported infrequently to date.Barbara et al. (1994) reported hyperpolarization-activatedchloride currents contributing both to the control ofmembrane potential and to osmotic balance regulation incarrot cells. Neither calcium ions nor MgATP werenecessary for fast activation of these channels. Underlarge hyperpolarization, Barbara et al. (1994) observedrapid and voltage-dependent channel inactivation.Recently, hyperpolarization-activated anion channels havealso been found in the plasmalemma of the unicellulargreen alga Eremosphaera viridis (SchoÈ nknecht et al., 1998).They conduct an anion e�ux and hence they are respons-ible for limiting the amplitude of dark-induced transienthyperpolarization caused by K�-release. The well-knownanion channel inhibitors such as A-9-C, NPPB and Zn2�block these channels. Elzenga and Van Volkenburgh(1997b) reported that in pea mesophyll cells there areCa2�-dependent anion currents activated by hyperpolar-izing pulses. These anion channels display ATP-dependentbi-modular ( fast and slow) kinetics. R-mode ( fast acti-vation and deactivation of the channel) occurs in theabsence of ATP. However when 3 mM MgATP is added tothe pipette solution facing the cytoplasmic side of themembrane, the current shows slow but clear time-inactivation (S-mode).

Dietrich and Hedrich (1994) showed the bimodularkinetics of the guard cell anion channel (GCAC1) in Viciafaba protoplasts. Previously these two modes of one guardcell anion channel were considered as two anion channels
contributing to di�erent depolarization-associated processes

extracellular face of the channel, eliciting stomatal opening.

kinase dependent anion uptake (Pei et al., 1996).

a

during regulation of stomatal movements (Schroeder andKeller, 1992). Dietrich and Hedrich (1994) noted that themode of action of GCAC1 is under the control ofcytoplasmic factors. Later Thomine et al. (1995) alsoidenti®ed a voltage-dependent anion channel in epidermalcells of Arabidopsis hypocotyls which showed two-modefunction: rapid and slow mode in the presence or absence ofintracellular ATP, respectively. R-type and S-type channelsare voltage-regulated in a quite di�erent way and theydisplay di�erent kinetics. Only R-type anion channelsdisplay strong voltage-dependence, while weak voltage-dependence of S-type channels leaves them partially activeeven when the membrane is strongly hyperpolarized. Suchbehaviour of S-type channels makes them responsible forsustained e�ux of anions (Keller et al., 1989; Linder andRaschke, 1992; Schroeder and Keller, 1992; Schroeder et al.,1993; Thomine et al., 1995), which serves as a negativeregulator during stomatal opening (Schroeder et al., 1993;Pei et al., 1998) or hypocotyl movements (Cho andSpalding, 1996). Transition between R- and S-mode of ananion channel may correspond to ATP binding (Schulz-Lessdorf et al., 1996; Thomine et al., 1997) or alternativelyto ATP-dependent phosphorylation/dephosphorylationprocesses (Schmidt et al., 1995; Thomine et al., 1995).R-type guard cell anion channels (GCAC1) in Arabidopsiswere shown not to be directly regulated by phosphorylationevents (Schulz-Lessdorf et al., 1996). They require cyto-plasmic ATP to undergo voltage- and Ca2�-dependentactivation, involving strongly cooperative binding of fourATP molecules (Schulz-Lessdorf et al., 1996). On the otherhand, S-type GCAC1 channels are strongly activated byphosphorylation (in Vicia faba and Commelina communisguard cells) or dephosphorylation (in Arabidopsis andNicotiana cells) (Armstrong et al., 1995; Schmidt et al.,1995; Cho and Spalding, 1996; Li and Assmann, 1996;Schulz-Lessdorf et al., 1996; Esser et al., 1997; Mori andMuto, 1997; Pei et al., 1997, 1998; Schwarz and Schroeder,1998). Therefore, guard cell anion channels characterized inArabidopsis (GCAC1) can also be classi®ed as ligand-gatedchannels, since Schulz-Lessdorf et al. (1996) showed directbinding of ATP to the channel protein. Leonhardt et al.(1999) in turn, suggest that the slow anion channel in guardcells may belong to the class of ATP binding cassette (ABC)proteins. The same situation applies in the case of voltage-gated and nucleotide-regulated anion channels of Arabi-dopsis hypocotyls described by Thomine et al. (1997). Theycon®rmed that nucleotide binding (ATP 4ADP�AMP)regulates channel activity (alters the kinetics and voltage-dependence, causing a shift toward depolarized potentialsand thus leading to a strong reduction of anion currentamplitude). This regulation may couple the electricalproperties of the membrane with the metabolic status ofthe whole cell.

Rapid- and slow-modes of the Arabidopsis guard cellanion channel (GCAC1) are also variously in¯uenced bypHcyt (Schulz-Lessdorf et al., 1996). The kinetics of S-modeis in¯uenced by the pH gradient across the plasmalemma(the inactivation gate responds to pH gradient, which maybe converted into a change of a channel structure). Such


pH gradient-dependence of slow inactivation resembles a

carrier-mode action. In the case of R-mode, the protongradient does not seem to a�ect channel activationfollowing ATP-binding. The single channel activity ofR-type GCAC1 increases as a function of [H�]cyt (proto-nation of the cytoplasmic site of the channel), while singlechannel conductance is una�ected either by pHcyt or pHext .Similar pH sensitivity was determined for anion-permeablevacuolar channels (Schulz-Lessdorf and Hedrich, 1995).Since the time- and voltage-dependent activity of guard cellanion channels (GCAC1) was shown to be stronglymodulated by ATP and H� (Schulz-Lessdorf et al., 1996),these channels have been thought to be capable of sensingchanges in the energy status, the proton pump activity andacid metabolism of the cell.

Patch-clamp studies revealed that growth hormones candirectly a�ect voltage-dependent activity of inwardlyrectifying anion channels in a dose-dependent manner(Hedrich and Jeromin, 1992). Auxin binding is side- andchannel-speci®c, and results in a shift of the activationpotentials towards the resting potential favouring transientchannel opening (Marten et al., 1991). These authorsdemonstrated that auxin can interact directly with the


Voltage-gated anion channels in the tonoplast

In the tonoplast (Table 3) there are two types of cytosol-negative-potential-activated (hyperpolarization-activated)anion channels: VCl and VMal (Allen and Sanders,1997). The ®rst is responsible for carrying Clÿ to thevacuole (inward rectifying), while the second is mainlypermeable for malate, but also for succinate, fumarate,acetate, oxaloacetate, NOÿ3 and H2PO

ÿ4 : VMal is very

strongly inward rectifying over the physiological range ofnegative potentials, but more negative than Emal (Ceranaet al., 1995). Cytosolic Ca2� and ATP do not a�ect VMalchannels (Cerana et al., 1995; Che�ngs et al., 1997). On theother hand, Pei et al. (1996) reported that calmodulin-likedomain protein kinase (CDPK) activates vacuolar malateand chloride conductances (VCl) in guard cell vacuoles ofVicia faba. Activation of both currents depends on Ca2�and ATP, enabling anion uptake into the vacuole even atphysiological potentials. CDPK-activated VCl currentswere also observed in red beet vacuoles, suggesting thatthese channels may provide a more general mechanism for

Voltage-dependent anion channels in other endomembranes

Voltage-dependent anion channels (VDACs or mitochon-drial porins) in the outer membrane of mitochondriaregulate the mitochondrial membrane potential, amongother things, during transduction of an apoptotic signal intothe cell (Green and Reed, 1998; Shimizu et al., 1999) ormetabolite di�usion (Elkeles et al., 1997; Rostovtseva andColombini, 1997; Mannella, 1998) (Table 3). According toRostovtseva and Colombini (1997) these channels areideally suited to controlling the ¯ow of ATP between thecytosol and the mitochondrial spaces. VDAC pore is formed
by a single �30-kDa protein (Song et al., 1998) which

ling cellular pH, transmembrane and osmotic potential.

a

undergoes a major conformational change at pH5 5(Mannella, 1997, 1998). However, functional VDAC is aheterodimer including one pore protein and other modulat-ing subunits (Elkeles et al., 1997). Apart from transmem-brane voltage and pH, VDACs can be regulated by directbinding of signalling proteins (Shimizu et al., 1999).

Anion uniport in plant mitochondria is mediated by apH-regulated inner membrane anion channel that is acti-vated by matrix H� (Beavis and Vercesi, 1992). Voltage-dependent inner mitochondrial anion channels (IMACs),which serve as a safeguard mechanism for recharging themitochondrial membrane potential, have been found inanimal tissues (Ballarin and Sorgato, 1996; Borecky et al.,1997).

Voltage-dependent anion channels were characterized bya patch-clamp study in osmotically swollen thylakoids fromPeperomia metallica (SchoÈ nknecht et al., 1988) and the algaNitellopsis obtusa (Pottosin and SchoÈ nknecht, 1995).Voltage-gated anion channels found in thylakoids are mostprobably responsible for the compensation of light-drivenH� movements (SchoÈ nknecht et al., 1988; Heiber et al.,1995).

Recently, Pohlmeyer et al. (1998) discovered a new typeof voltage-dependent solute channel of high conductance inthe outer envelope of chloroplasts, etioplasts and non-greenroot plastids (Table 3). The channels are permeable fortriosephosphate, ATP, Pi , dicarboxylic acids, amino acids,and sugars. Their open probability is highest at 0 mV (whichis consistent with the absence of transmembrane potentialacross the plastidic outer membranes). Previously, Heiberet al. (1995) reported a voltage-dependent anion channel oflow conductance in the chloroplast envelope. There are alsoanion channels found in the inner envelope membrane of


isolated intact chloroplasts (Fuks and Homble, 1999).

growth and development.

Stretch-activated anion channels

Falke et al. (1988) ®rst reported large conductance,stretch-activated, anion-selective channels in protoplasts oftobacco. Cosgrove and Hedrich (1991) then showed theexistence of stretch-activated Clÿ, Ca2� and K� channels inthe plasma membrane of guard cells. Teodoro et al. (1998)suggested that the changes in turgor pressure induced byhyper-/hypo-osmotic stress may cause an early inactivation/
activation of stretch-sensitive anion channels, respectively.
from the State Committee for Scienti®c Research.

vacuoles by cytosolic and luminal calcium. The Plant Journal 10:

Light-activated anion channels

By patch clamping hypocotyl cells isolated from dark-grown Arabidopsis thaliana seedlings, Cho and Spalding(1996) revealed the existence of blue-light activated anionchannels responsible for light induced membrane depolar-ization (Table 2). Their results are consistent with previousreports of Elzenga et al. (1995). Further studies on blue-light activated anion channels in Arabidopsis hypocotylconducted by Lewis et al. (1997) showed that the openprobability of the channel depends on [Ca2�]cyt and thatwithin the calcium concentration range of 1±10 mM theprobability of channel activation increases. Their results
indicate that cytoplasmic calcium does not a�ect the anion
channel directly, but that it does so through intermediates(e.g. Ca2�-dependent kinases or phosphatases). Activationof blue light-induced anion channels plays a central role intransducing light signals into hypocotyl growth inhibition(Cho and Spalding, 1996; Parks et al., 1998).

Light-activated anion channels, resembling those above,were also reported by Elzenga and Van Volkenburgh(1997a) (Table 2). They examined light-induced transientdepolarization in Pisum sativum mesophyll cells due toincreased conductance for anions and concluded that:(1) under illumination the anion current increases three-fold because of an increase in the open probability of a 32-pS anion channel; (2) this change in channel activity is notdue to light-induced changes in membrane potential; (3) theanion current depends on light intensity and can be totallyblocked by the photosynthetic inhibitor DCMU; (4) theanion current is strongly Ca2�-dependent; and (5) light-induced anion e�ux may balance light-induced protonextrusion and therefore participate in a mechanism control-


CONCLUSIONS

From year to year the number of characterized ion channelsincreases, which bene®ts our understanding of their roles innumerous physiological processes. Modern electrophysio-logical and molecular biological techniques have enabledthe characterization and classi®cation of novel channeltypes. On the other hand, some channels previouslydescribed as di�erent types are in fact `synonyms'. Thesemainly originate from multiple gating mechanisms that cansense the energy status of the cell and thus make the cellresponsive to various stimuli in a very e�cient way. The ®netuning of channel activities depends on e�ectors availablein a certain cell type, i.e. it is plant and tissue speci®c(Barbier-Brygoo et al., 1999). Further research concerningregulation and gating of the ion channels described here willhelp to unravel the intermediate signalling mechanisms usedby plants in dynamic responses to the environment during

ACKNOWLEDGEMENTS

We thank Professor M. A. Venis and the reviewers forhelpful comments and critical reading of the manuscript.The investigation was supported by the grant 6P04 C 04218

LITERATURE CITED

Allan AC, Fricker MD, Ward JL, Beale MH, Trewavas AJ. 1994. Twotransduction pathways mediate rapid e�ects of abscisic acid inCommelina guard cells. The Plant Cell 6: 1319±1328.

Allen JE, Sanders D. 1994. Voltage-gated Ca2� release channels invacuolar membranes from beet storage roots and guard cells.Symposia of the Society for Experimental Botany 48: 113±122.

Allen GJ, Sanders D. 1995. Calcineurin, a type 2B protein phosphatase,modulates the Ca2�-permeable slow vacuolar ion channel ofstomatal guard cells. The Plant Cell 7: 1473±1483.

Allen GJ, Sanders D. 1996. Control of ionic currents in guard cells

1055±1069.

a

Allen GJ, Sanders D. 1997. Vacuolar ion channels of higher plants.Advances in Botanical Research Incorporating Advances in PlantPathology 3914: 217±252.

Allen GJ, Amtmann A, Sanders D. 1998a. Calcium-dependent andcalcium-independent K� mobilization channels in Vicia fabaguard cell vacuoles. Journal of Experimental Botany 49: 305±318.

Allen GJ, Muir SR, Sanders D. 1995. Release of Ca2� from individualplant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268:735±737.

Allen GJ, Sanders D, Gradmann D. 1998b. Calcium±potassiumselectivity: kinetic analysis of current±voltage relationships ofthe open, slowly activating channel in the vacuolar membrane ofVicia faba guard-cells. Planta 204: 528±541.

Armstrong F, Leung J, Grabov A, Brearley J, Giraudat J, Blatt MR.1995. Sensitivity to ABA of guard cell K� channels is suppressedby abi 1-1, a mutant Arabidopsis gene encoding a putative proteinphosphatase. Proceedings of the National Academy of Sciences,USA 92: 9520±9524.

Ballarin C, Sorgato MC. 1996. Anion channels of the inner membraneof mammalian and yeast mitochondria. Journal of Bioenergeticsand Biomembranes 28: 125±130.

Barbara J-G, Stoeckel H, Takeda K. 1994.Hyperpolarization-activatedinward current in protoplasts from suspension-cultured carrotcells. Protoplasma 180: 136±144.

Barbier-Brygoo H, Frachisse JM, Colcombet J, Thomine S. 1999.Anion channels and hormone signalling in plant cells. PlantPhysiology and Biochemistry 37: 381±392.

Bauer CS, Plieth C, Bethmann B, Popescu O, Hansen UP, Simonis W,SchnoÈ knecht G. 1998. Strontium-induced repetitive calcium spikesin a unicellular green alga. Plant Physiology 117: 545±557.

Beavis AD, Vercesi AE. 1992. Anion uniport in plant mitochondria ismediated by a Mg2�-insensitive inner membrane anion channel.The Journal of Biological Chemistry 267: 3079±3087.

Becker D, Dreyer I, Hoth S, Reid JD, Bush H, Lehnen M, Palme K,Hedrich R. 1996. Changes in voltage activation, Cs� sensitivityand ion permeability in H5 mutants of the plant K� channelsKAT1. Proceedings of the National Academy of Sciences, USA 93:8123±8128.

Bei QX, Luan S. 1998. Functional expression and characterization of aplant K� channel gene in a plant cell model. The Plant Journal 13:857±865.

Berry AW, Cowan DSC, Harpham NVJ, Hemsley RJ, Novikova GV,Smith AR, Hall MA. 1996. Studies on the possible role of proteinphosphorylation in the transduction of the ethylene signal. PlantGrowth Regulation 18: 135±141.

Bertl A, Reid JD, Sentenac H, Slayman CL. 1997. Functionalcomparison of plant inward-recti®er channels expressed in yeast.Journal of Experimental Botany 48: 405±413.

Bethke PC, Jones RL. 1997. Reversible protein phosphorylationregulates the activity of the slow-vacuolar channel. The PlantJournal 11: 1227±1235.

Biswas S, Dalal B, Sen M, Biswas BB. 1995. Receptor for myoinositoltriphosphate from the microsomal fraction of Vigna radiata.Biochemistry Journal 306: 631±636.

Blatt MR. 1999. Reassessing roles for Ca2� in guard cell signalling.Journal of Experimental Botany 50: 989±999.

Blatt MR, Grabov A. 1997a. Signalling gates in abscisic acid-mediatedcontrol of guard cell ion channels. Physiologia Plantarum 100:481±490.

Blatt MR, Grabov A. 1997b. Signal redundancy, gates and integrationin the control of ion channels for stomatal movement. Journal ofExperimental Botany 48: 529±537.

Blatt MR, Thiel G. 1994.K� channels of stomatal guard cells. Bimodalcontrol of the K� inward recti®er evoked by auxin. The PlantJournal 5: 55±68.

Blatt MR, Thiel G, Trentham D. 1990. Reversible inactivation of K�channels of Vicia stomatal guard cells following the photolysis ofcaged inositol 1,4,5-triphosphate. Nature 346: 766±769.

Blom-Zandstra M, Koot H, van Hattum J, Vogelzang SA. 1997.Transient light induced changes in ion channel and proton pump


activities in the plasma membrane of tobacco mesophyll proto-plasts. Journal of Experimental Botany 48: 1623±1630.

Blumwald E, Aharon GS, Lam BC-H. 1998. Early signal transductionpathways in plant±pathogen interactions. Trends in Plant Science3: 342±346.

Borecky J, Jezek P, Siemen D. 1997. 108-pS channel in brown fatmitochondria might be identical to the inner membrane anionchannel. The Journal of Biological Chemistry 272: 19282±19289.

Braun DM, Walker JC. 1996. Plant transmembrane receptors: newpieces in the signalling puzzle. Trends in Biochemical Sciences 21:70±73.

Brownlee C, Goddard H, Hetherington AM, Peake L-A. 1999.Speci®city and integration of responses: Ca as a signal in polarityand osmotic regulation. Journal of Experimental Botany 50:1001±1011.

BruÈ ggemann LI, Pottosin II, SchoÈ nknecht G. 1999a. Cytoplasmicmagnesium regulates the fast activating vacuolar cation channel.Journal of Experimental Botany 50: 1547±1552.

BruÈ ggemann LI, Pottosin II, SchoÈ nknecht G. 1999b. Selectivity of thefast activating vacuolar cation channel. Journal of ExperimentalBotany 50: 873±876.

Carpaneto A, Cantu AM, Gambale F. 1999. Redox agents regulateactivity in vacuoles from higher plant cells. FEBS Letters 442:129±132.

Cerana R, Giromini L, Colombo R. 1995. Malate-regulated channelspermeable to anions in vacuoles of Arabidopsis thaliana. PlantPhysiology 22: 115±121.

Cerana R, Giromini L, Colombo R. 1999. On the gating mechanism ofthe slowly activating vacuolar channels of Arabidopsis thalianacultured cells. Journal of Plant Physiology 154: 617±622.

Che�ngs CM, Pantoja O, Ashcroft F, Smith JAC. 1997. Malatetransport and vacuolar ion channels in CAM plants. Journal ofExperimental Botany 48: 623±631.

Cho MH, Spalding EP. 1996. An anion channel in Arabidopsishypocotyls activated by blue light. Proceedings of the NationalAcademy of Sciences, USA 93: 8134±8138.

Claussen M, LuÈ then H, Blatt M, BoÈ ttger M. 1997. Auxin-inducedgrowth and its linkage to potassium channels. Planta 201:227±234.

Cosgrove DJ, Hedrich R. 1991. Stretch-activated Clÿ, K� and Ca2�channels co-existing in plasma membrane of guard cells of Viciafaba L. Planta 186: 143±153.

Czempinski K, Gaedeke N, Zimmermann S, MuÈ ller-RoÈ ber B. 1999.Molecular mechanisms and regulation of plant ion channels.Journal of Experimental Botany 50: 955±966.

Czempinski K, Zimmermann S, Ehrhardt T, MuÈ ller-RoÈ ber B. 1997.Newstructure and function in plant K� channels: KCO1, an outwardrecti®er with a steep-dependency. The EMBO Journal 16:2565±2575.

Davies E. 1993. Intercellular and intracellular signals and theirtransduction via the plasma membrane±cytoskeleton interface.Seminars in Cell Biology 4: 139±147.

De Boer B. 1997. FusicoccinÐa key to multiple 14-3-3 locks?. Trends inPlant Science 2: 60±66.

De Boer AH, Wegner LH. 1997. Regulatory mechanisms of ionchannels in xylem parenchyma cells. Journal of ExperimentalBotany 48: 441±449.

Dietrich P, Hedrich R. 1994. Interconversion of fast and slow modes ofGCAC1, a guard cell anion channel. Planta 195: 301±304.

Dobrovinskaya OR, Muniz J, Pottosin II. 1999. Inhibition of vacuolarion channels by polyamines. Journal of Membrane Biology 167:127±140.

Dreyer I, Antunes S, Hoshi T, MuÈ ller-RoÈ ber B, Palme K, Pongs O,Reintanz B, Hedrich R. 1997. Plant K� channel a-subunitsassemble indiscriminately. Biophysical Journal 72: 2143±2150.

Eckert M, Biela A, Siefritz F, Kaldenho� R. 1999. New aspects of plantregulation and speci®city. Journal of Experimental Botany 50:1541±1545.

Elkeles A, Breiman A, Zizi M. 1997. Functional di�erences amongwheat voltage-dependent anion channel (VDAC) isoformsexpressed in yeastÐidenti®cation for the presence of a novel


VDAC-modulating protein?. The Journal of Biological Chemistry272: 6252±6260.

a

Elzenga JTM, Van Volkenburgh E. 1997a. Characterization of a light-controlled anion channel in the plasma membrane of mesophyllcells of pea. Plant Physiology 113: 1419±1426.

Elzenga JTM, Van Volkenburgh E. 1997b. Kinetics of Ca2�- and ATP-dependent, voltage-controlled anion conductance in the plasmamembrane of mesophyll cells of Pisum sativum. Planta 201:415±425.

Elzenga JTM, Prins HBA, Van Volkenburgh E. 1995. Light-inducedmembrane potential changes of epidermal and mesophyll cells ingrowing leaves of Pisum sativum. Planta 197: 127±134.

Elzenga JTM, Staal M, Prins HBA. 1997. Calcium-calmodulin signal-ling is involved in light-induced acidi®cation by epidermal leafcells of pea, Pisum sativum L. Journal of Experimental Botany 48:2055±2060.

Ermolayeva E, Sanders D, Johannes E. 1997. Ionic mechanism and roleof phytochrome-mediated membrane depolarisation in caulone-mal side branch initial formation in the moss Physcomitrellapatens. Planta 201: 109±118.

Ermolayeva E, Hohmeyer H, Johannes E, Sanders D. 1996. Calcium-dependent membrane depolarisation activated by phytochrome inthe moss Physcomitrella patens. Planta 199: 352±358.

Esser J, Liao Y-J, Schroeder JI. 1997. Characterization of ion channelmodulator e�ects on ABA- and malate-induced stomatal move-ments: strong regulation by kinase and phosphatase inhibitors andrelative insensitivity to mastoparans. Journal of ExperimentalBotany 48: 539±550.

Fairley-Grenot KA, Assmann SM. 1992. Permeation of Ca2� throughK� channels in the plasma membrane of Vicia faba guard cells.Journal of Membrane Biology 128: 103±113.

Falke LC, Edwards KL, Pickard BG, Misler S. 1988. A stretch-activated anion channel in tobacco protoplast. FEBS Letters 237:141±144.

Fuks B, Homble F. 1999. Passive anion transport through thechloroplast inner envelope membrane measured by osmoticswelling of intact chloroplasts. Biochimica et Biophysica ActaÐBiomembranes 1416: 361±369.

Galione A, Summerhill R. 1996. Regulation of ryanodine receptors bycyclic ADP-ribose. In: Soretino V, ed. Ryanodine receptors.Boca Raton, Florida: CRC Press, 52±70.

Gambale F, Bergante M, Stragapede F, Cantu AM. 1996. Ionicchannels of the sugar beet tonoplast are regulated by a multi-ionsingle-®le permeation mechanism. Journal of Membrane Biology154: 69±79.

Gaymard F, Pilot G, Lacombe B, Bouchez D, Michaux-Ferriere N,Thibaud JB, Sentenac H. 1998. Identi®cation and disruption of aplant shaker-like outward channel involved in K� release into thexylem sap. Cell 94: 647±655.

Gelli A, Blumwald E. 1997. Hyperpolarization-activated Ca2� per-meable channels in the plasma membrane of tomato cells. Journalof Membrane Biology 155: 35±45.

Grabov A, Blatt MR. 1997. Parallel control of the inward-recti®er K�channel by cytosolic free Ca2� and pH in Vicia guard cells. Planta201: 84±95.

Grabov A, Blatt MR. 1998a. Co-ordination of signalling elements inguard cell ion control. Journal of Experimental Botany 49:351±360.

Grabov A, Blatt MR. 1998b. Membrane voltage initiates Ca2� wavesand potentiates Ca2� increases with abscisic acid in stomatalguard cells. Proceedings of the National Academy of Sciences, USA95: 4778±4783.

Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science 281:1309±1312.

Grygorczyk C, Grygorczyk RA. 1998. Ca2�- and voltage-dependentcation channel in the nuclear envelope of red beet. Biochimica etBiophysica ActaÐBiomembranes 1375: 117±130.

Hedrich R, Dietrich P. 1996. Plant K� channels: similarity anddiversity. Botanica Acta 109: 94±101.

Hedrich R, Jeromin A. 1992. A new scheme of symbiosis: ligand- andvoltage- gated anion channels in plants and animals. Philosophical


Transactions of the Royal Society of LondonÐSeries B: BiologicalScience 338: 31±38.

Hedrich R, Bush H, Raschke K. 1990. Ca2� and nucleotide dependentregulation of voltage dependent anion channels in the plasmamembrane of guard cells. The EMBO Journal 9: 3889±3892.

Heiber T, Steinkamp T, Hinnah S, Schwarz M, FluÈ gge UI, Weber A,Wagner R. 1995. Ion channels in the chloroplast envelopemembrane. Biochemistry-US 34: 15906±15917.

Hinnah SC, Wagner R. 1998. Thylakoid membranes contain a high-conductance channel. European Journal of Biochemistry 253:606±613.

Holdaway-Clarke TL, Feijo JA, Hackett GR, Kunkel JG, Hepler PK.1997. Pollen tube growth and the intracellular cytosolic calciumgradient oscillate in phase while extracellular calcium in¯ux isdelayed. The Plant Cell 9: 1999±2010.

Hoshi T. 1995. Regulation of voltage dependence of the KAT1 channelby the intracellular factors. Journal of General Physiology 105:309±328.

Hoth S, Dreyer I, Dietrich P, Becker D, MuÈ ller-RoÈ ber B, Hedrich R.1997. Molecular basis of plant-speci®c acid activation of K�uptake channels. Proceedings of the National Academy of Sciences,USA 94: 4806±4810.

Hwang JU, Suh S, Yi H, Kim J, Lee Y. 1997. Actin ®laments modulateboth stomatal opening and inward K� channel activities in guardcells of Vicia faba L. Plant Physiology 115: 335±342.

Iijima T, Hagiwara S. 1987. Voltage-dependent K channels in proto-plasts of Dionaea muscipula. Journal of Membrane Biology 100:73±81.

Iijima T, Sibaoka T. 1985. Membrane potentials in excitable cells ofAldrovanda vesiculosa trap-lobes. Plant Cell Physiology 26: 1±13.

Ilan N, Schwartz A, Moran N. 1996. External protons enhance theactivity of the hyperpolarization-activated K� channels in guardcell protoplasts of Vicia faba. Journal of Membrane Biology 154:169±181.

Jan LY, Jan YN. 1997. Receptor-regulated ion channels. CurrentOpinion in Cell Biology 9: 155±160.

Jin X-C, Wu W-H. 1999. Involvement of cyclic AMP in ABA- andCa2�-mediated signal transduction of stomatal regulation in Viciafaba. Plant Cell Physiology 40: 1127±1133.

Johannes E, Sanders D. 1995. Luminal calcium modulates unitaryconductance and gating of an endomembrane calcium releasechannel. Journal of Membrane Biology 146: 211±224.

Johannes E, Crofts A, Sanders D. 1998. Control of Clÿ e�ux in Characorallina by cytosolic pH, free Ca2�, and phosphorylationindicates a role of plasma membrane anion channels in cytosolicpH regulation. Plant Physiology 118: 173±181.

Johansson I, Larsson C, Ek B, Kjellbom P. 1996. The major integralproteins of spinach leaf plasma membranes are putative aqua-porins and are phosphorylated in response to Ca2� and apoplasticwater potential. The Plant Cell 8: 1181±1191.

Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C,Kjellbom P. 1998. Water transport activity of the plasmamembrane aquaporin PM28A is regulated by phosphorylation.The Plant Cell 10: 451±459.

Katsuhara M, Tazawa M. 1992. Calcium-regulated channels and theirbearing on physiological activities in Characean cells. Philo-sophical Transactions of the Royal Society of London 338: 19±29.

Katsuhara M, Mimura T, Tazawa M. 1990. ATP-Regulated ionchannels in the plasma membrane of Characeae alga, Nitellopsisobtusa. Plant Physiology 93: 343±346.

Keller BU, Hedrich R, Raschke K. 1989. Voltage-dependent anionchannels in the plasma membrane of guard cells. Nature 341:450±453.

Kiegle E, Gilliham M, Haselo� J, Tester M. 2000. Hyperpolarisation-activated calcium currents found only in cells from elongationzone of Arabidopsis thaliana roots. Plant Journal 21: 225±229.

Kim HY, Cote GC, Crain RC. 1992. E�ects of light on the membranepotential of protoplasts from Samanea saman pulvini. PlantPhysiology 99: 1532±1539.

Kim HY, Cote GC, Crain RC. 1996. Inositol 1,4,5-triphosphate maymediate closure of K� channels by light and darkness in Samaneasaman motor cells. Planta 198: 279±287.


Kinoshita T, Shimazaki K. 1997. Involvement of calyculin A- andokadaic acid-sensitive protein phosphatase in the blue light

a

response of stomatal guard cells. Plant Cell Physiology 38:1281±1285.

KluÈ sener B, Boheim G, Weiler EW. 1997. Modulation of the ER Ca2�-channel BBC1 from tendrils of Bryonia diodica by divalentcations, protons and H2O2. FEBS Letters 407: 230±234.

KluÈ sener B, Boheim G, Li BH, Engelberth J, Weiler EW. 1995.Gadolinium-sensitive voltage-dependent calcium release channelsin the endoplasmic reticulum of a higher plant mechanoreceptororgan. The EMBO Journal 14: 2708±2714.

Knight H, Trewavas AJ, Knight MR. 1996. Cold calcium signalling inArabidopsis involves two cellular pools and a change in calciumsignature after acclimation. The Plant Cell 8: 489±503.

Kourie JI. 1996. Interaction of extracellular potassium and caesiumwith the kinetics of inward rectifying K� channels in the plasmamembrane of mesophyll protoplasts of Avena sativa. Plant CellPhysiology 37: 770±781.

Kurosaki F. 1997. Role of inward K� channel located at carrot plasmamembrane in signal cross-talking of cAMP with Ca2� cascade.FEBS Letters 408: 115±119.

Lacombe B, Pilot G, Gaymard F, Sentenac H, Thibaud JB. 2000.pH control of the outwardly-rectifying potassium channel SKOR.FEBS Letters 466: 351±354.

Lee HC. 2000. NAADP: An emerging calcium signaling molecule.Journal of Membrane Biology 173: 1±8.

Leckie CP, McAinsh MR, Montgomery L, Priestley AJ, Staxen I, WebbAAR, Hetherington AM. 1998. Second messengers in guard cells.Journal of Experimental Botany 49: 339±349.

Leonhardt N, Vavasseur A, Forestier C. 1999. ATP binding cassettemodulators control abscisic acid-regulated slow anion channels inguard cells. The Plant Cell 11: 1141±1151.

Lewis BD, Karlin-Neumann G, Davis RW, Spalding EP. 1997. Ca2�-activated anion channels and membrane depolarizations inducedby blue light and cold in Arabidopsis seedlings. Plant Physiology114: 1327±1334.

Li W, Assmann SM. 1993. Characterization of a G-protein-regulatedoutward K� current in mesophyll cells of Vicia faba L. Proceed-ings of the National Academy of Sciences, USA 90: 262±266.

Li J, Assmann SM. 1996. An abscisic acid-activated and calcium-independent protein kinase form guard cells of fava bean. ThePlant Cell 8: 2359±2368.

Li J, Lee YRJ, Assmann S. 1998. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potas-sium channel. Plant Physiology 116: 785±795.

Linder B, Raschke K. 1992. A slow anion channel in guard cells,activating at large hyperpolarization, may be principal forstomatal closing. FEBS Letters 313: 27±30.

Linz KW, KoÈ hler K. 1994. Vacuolar ion currents in the primitive greenalga Eremosphaera viridis: the electrical properties are suggestiveof both the Characeae and higher plants. Protoplasma 179: 34±45.

Liu K, Luan S. 1998. Voltage-dependent K� channels as targets ofosmosensing in guard cells. The Plant Cell 10: 1957±1970.

Logan H, Basset M, Very AA, Sentenac H. 1997. Plasma membranetransport systems in higher plants: from black boxes to molecularphysiology. Physiologia Plantarum 100: 1±15.

LuÈ hring H. 1999. pH-sensitive gating kinetics of the maxi-K channel inthe tonoplast of Chara australis. Journal of Membrane Biology168: 47±61.

McAinsh MR, Brownlee C, Hetherington AM. 1997. Calcium ions assecond messengers in guard cell signal transduction. PhysiologiaPlantarum 100: 16±29.

McAinsh MR, Webb AR, Taylor JE. 1995. Stimulus inducedoscillations in guard cell cytosolic free calcium. The Plant Cell 7:1207±1219.

Maathuis FJM, Ichida AM, Sanders D, Schroeder JI. 1997. Roles ofhigher plant K� channels. Plant Physiology 114: 1141±1149.

MacRobbie EAC. 1997. Signal transduction and ion channels in guardcells. Journal of Experimental Botany 48: 515±528.

Mannella CA. 1997. On the structure and gating mechanism of themitochondrial channel, VDAC. Journal of Bioenergetics andBiomembranes 29: 525±531.

Mannella CA. 1998. Conformational changes in the mitochondrial


channel protein, VDAC, and their functional implications.Journal of Structural Biology 121: 207±218.

Marten I, Lohse G, Hedrich R. 1991. Plant growth hormones controlvoltage-dependent activity of anion channels in plasma membraneof guard cells. Nature 353: 758±762.

Mayer WE, Hohloch C, Kalkuhl A. 1997. Extensor protoplasts of thePhaseolus pulvinus: Light-induced swelling may require extra-cellular Ca2� in¯ux, dark-induced shrinking inositol 1,4,5-trisphosphate-induced Ca2� mobilization. Journal of ExperimentalBotany 48: 219±228.

Moran N. 1996. Membrane-delimited phosphorylation enables theactivation of the outward-rectifying K channels in motor cellprotoplasts of Samanea saman. Plant Physiology 111: 1281±1292.

Mori IC, Muto S. 1997. Abscisic acid activates a 48-kDa protein kinasein guard cell protoplasts. Plant Physiology 113: 833±840.

Muir SR, Sanders D. 1996. Pharmacology of Ca2� release from redbeet microsomes suggests the presence of ryanodine receptorhomologs in higher plants. FEBS Letters 255: 92±96.

Muir SR, Sanders D. 1997. Inositol 1,4,5-trisphosphate-sensitive Ca2�release across nonvacuolar membranes in cauli¯ower. PlantPhysiology 114: 1511±1521.

Muir SR, Bewell MA, Sanders D, Allen GJ. 1997. Ligand-gated Ca2�channels and signalling in higher plants. Journal of ExperimentalBotany 48: 589±597.

MuÈ ller-RoÈ ber B, Ellenberg J, Provart N, Willmitzer L, Bush H, BeckerD, Dietrich P, Hoth S, Hedrich R. 1995. Cloning and electro-physiological analysis of KST1, an inward-rectifying K� channelexpressed in potato guard cells. The EMBO Journal 14:2409±2416.

Okihara K, Ohkawa T, Tsutsui I, Kasai M. 1991. A Ca2�- and voltage-dependent Clÿ-sensitive anion channels in the Chara plasma-lemma: patch-clamp study. Plant Cell Physiology 32: 593±601.

Parks BM, Cho MH, Spalding EP. 1998. Two genetically separablephases of growth inhibition induced by blue light in Arabidopsisseedlings. Plant Physiology 118: 609±615.

Pei ZH, Schroeder JI, Schwarz M. 1998. Background ion channelactivities in Arabidopsis guard cells and review of ion channelregulation by protein phosphorylation events. Journal of Experi-mental Botany 49: 319±328.

Pei ZM, Ward JM, Harper JF, Schroeder JI. 1996. A novel chloridechannel in Vicia faba guard cell vacuoles activated by the Ser/Thrkinase, CDPK. The EMBO Journal 15: 6564±6574.

Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder JI. 1997.Di�erential abscisic acid regulation of guard cell slow anionchannels in Arabidopsis wild-type and abi 1 and abi 2 mutants.The Plant Cell 9: 409±423.

Pineros M, Tester MA. 1997. Calcium channels in higher plant cells:selectivity, regulation and pharmacology. Journal of ExperimentalBotany 48: 551±577.

Pohlmeyer K, Soll J, Grimm R, Hill K, Wagner R. 1998. A high-conductance solute channels in the chloroplastic outer envelopefrom pea. The Plant Cell 10: 1207±1216.

Pottosin II, SchoÈ nknecht G. 1995. Patch clamp study of the voltage-dependent anion channel in the thylakoid membrane. Journal ofMembrane Biology 148: 143±156.

Pottosin II, SchoÈ nknecht G. 1996. Ion channel permeable for divalentand monovalent cations in native spinach thylakoid membranes.Journal of Membrane Biology 152: 223±233.

Pottosin II, Tikhonova LI, Hedrich R, SchoÈ nknecht G. 1997. Slowlyactivating vacuolar channels can not mediate Ca2�-induced Ca2�release. The Plant Journal 12: 1387±1398.

Ramahaleo T, Alexandre J, Lassalles JP. 1996. Stretch activatedchannels in plant cells: A new model for symplastic coupling.Plant Physiology and Biochemistry 34: 327±334.

Reid RJ, Tester MA, Smith FA. 1997. Voltage control of calcium in¯uxin intact cells. Australian Journal of Plant Physiology 24: 805±810.

Roberts SK, Tester M. 1995. Inward and outward K� selective currentsin the plasma membrane of protoplasts from maize root cortexand stele. The Plant Journal 8: 811±825.

Rostovtseva T, Colombini M. 1997. VDAC channels mediate and gatethe ¯ow of ATP: implications for the regulation of mitochondrialfunction. Biophysical Journal 72: 1954±1962.


Sanders D, Brownlee C, Harper JF. 1999. Communicating withcalcium. The Plant Cell 11: 691±706.

a

Schmidt C, Schelle I, Liao Y-I, Schroeder JI. 1995. Strong regulation ofslow anion channels and abscisic acid signalling in guard cells byphosphorylation and dephosphorylation events. Proceedings ofthe National Academy of Sciences, USA 92: 9535±9539.

SchoÈ nknecht G, Bauer CS, Simonis W. 1998. Light-dependent signaltransduction and transient changes in cytosolic Ca2� in aunicellular green alga. Journal of Experimental Botany 49: 1±11.

SchoÈ nknecht G, Hedrich R, Junge W, Raschke K. 1988. A voltage-dependent chloride channel in the photosynthetic membrane of ahigher plant. Nature 336: 589±592.

Schroeder JI. 1989. Quantitative analysis of outward rectifying K�channel currents in guard cell protoplasts from Vicia faba. Journalof Membrane Biology 107: 229±235.

Schroeder JI, Keller BU. 1992. Two types of anion channel currents inguard cells with distinct voltage regulation. Proceedings of theNational Academy of Sciences, USA 89: 5025±5029.

Schroeder JI, Hedrich R, Fernandez JM. 1984. Potassium-selectivesingle channels in guard cell protoplasts of Vicia faba. Nature 312:361±362.

Schroeder JI, Schmidt C, Shea�er J. 1993. Identi®cation of high-a�nity slow anion channel blockers and evidence for stomatalregulation by slow anion channels in guard cells. The Plant Cell 5:1831±1841.

Schulz-Lessdorf B, Hedrich R. 1995. Protons and calcium modulateSV-type channels in the vacuolar-lysosomal compartmentÐchannel interaction with calmodulin inhibitors. Planta 197:655±671.

Schulz-Lessdorf B, Lohse G, Hedrich R. 1996. GCAC1 recognises thepH gradient across the plasma membrane: a pH-sensitive andATP-dependent anion channels links guard cell membranepotential to acid and energy metabolism. The Plant Journal 10:993±1004.

Schumaker KS, Gizinski MJ. 1993. Cytokinin stimulatesdihydropyridine-sensitive calcium uptake in moss protoplasts.Proceedings of the National Academy of Sciences, USA 90:10937±10941.

Schwarz M, Schroeder JI. 1998. Abscisic acid maintains S-type anionchannel activity in ATP-depleted Vicia faba guard cells. FEBSLetters 428: 177±182.

Shimizu S, Narita M, Tsujimoto Y. 1999. Bcl-2 family proteins regulatethe release of apoptotic cytochrome c by the mitochondrialchannel VDAC. Nature 399: 483±487.

Shimmen T. 1997. Studies on mechanoperception in characean cells:pharmacological analysis. Plant Cell Physiology 38: 139±148.

Sidler M, Hassa P, Hasan S, Ringli C, Dudler D. 1998. Involvement ofan ABC transporter in a developmental pathway regulating hypo-cotyl cell elongation in the light. The Plant Cell 10: 1623±1636.

Sievers A, Buchen B, Hodick D. 1996. Gravity sensing in tip-growingcells. Trends in Plant Science 1: 273±279.

Song JM, Midson C, Blachy-Dyson E, Forte M, Colombini M. 1998.The topology of VDAC as probed by biotin modi®cation. TheJournal of Biological Chemistry 273: 24406±24413.

Stoeckel H, Takeda K. 1993. Plasmalemmal, voltage-dependent ioniccurrents from excitable pulvinar motor cells of Mimosa pudica.Journal of Membrane Biology 131: 179±192.

Stoeckel H, Takeda K. 1995. Calcium sensitivity of the plasmalemmaldelayed recti®er potassium current suggests that calcium in¯ux inpulvinar protoplasts from Mimosa pudica L can be revealed byhyperpolarization. Journal of Membrane Biology 146: 201±209.

Stone JM, Walker JC. 1995. Plant protein kinase families and signaltransduction. Plant Physiology 108: 451±457.

Suh SJ, Park J, Lee Y. 1998. Possible involvement of phospholipaseA2 in light signal transduction of guard cells of Commelinacommunis. Physiologia Plantarum 104: 306±310.

Szarek I, Trebacz K. 1999. The role of light-induced membranepotential changes in guttation in gametophytes of Aspleniumtrichomanes. Plant Cell Physiology 40: 1280±1286.

Tang H, Vasconcelos AC, Berkowitz GA. 1996. Physical association ofKAB1 with plant K� channel a subunit proteins. The Plant Cell 8:1545±1553.

Tang H, Vasconcelos AC, Ma J, Berkowitz GA. 1998. In vivo expression�


pattern of a plant K channel b subunit protein. Plant Science134: 117±128.

Taylor AR, Manison NFH, Fernandez C, Wood J, Browlee C. 1996.Spatial organisation of calcium signalling involved in cell volumecontrol in the Fucus rhizoid. The Plant Cell 8: 2015±2031.

Teodoro AE, Zingarelli L, Lado P. 1998. Early changes of Clÿ e�uxand H� extrusion induced by osmotic stress in Arabidopsisthaliana cells. Physiologia Plantarum 102: 29±37.

Thiel G, Brudern A, Gradmann D. 1996. Small inward rectifying K�channels in coleoptiles: Inhibition by external Ca2� and functionin cell elongation. Journal of Membrane Biology 149: 9±20.

Thiel G, Homann U, Gradmann D. 1993. Microscopic elements ofelectrical excitation in Chara: transient activity of Clÿ channels inthe plasma membrane. Journal of Membrane Biology 134: 53±66.

Thion L, Mazars C, Thuleau P, Graziana A, Rossigud M, Moreau M,Ranjeva R. 1996. Activation of plasma membrane voltage-dependent calcium-permeable channels by disruption of micro-tubules in carrot cells. FEBS Letters 393: 13±18.

Thomine S, Guern J, Barbier-Brygoo H. 1997. Voltage-dependentanion channel of Arabidopsis hypocotyls: Nucleotide regulationand pharmacological properties. Journal of Membrane Biology159: 71±82.

Thomine S, Zimmermann S, Guern J, Barbier-Brygoo H. 1995. ATP-dependent regulation of an anion channel at the plasmamembrane of protoplasts from epidermal cells of Arabidopsishypocotyls. The Plant Cell 7: 2091±2100.

Thuleau P, Ward JM, Ranjeva R, Schroeder JI. 1994. Voltage-dependent calcium-permeable channel in the plasma membraneof a higher plant cell. The EMBO Journal 13: 2970±2975.

Tikhonova LI, Pottosin II, Dietz KJ, SchoÈ nknecht G. 1997. Fast-activating cation channel in barley mesophyll vacuoles. Inhibitionby calcium. The Plant Journal 11: 1059±1070.

Trebacz K, Simonis W, SchoÈ nknecht G. 1994. Cytoplasmic Ca2�, K�,Clÿ and NOÿ3 activities in the liverwort Conocephalum conicum atrest and during action potentials. Plant Physiology 106:1073±1084.

Trewavas AJ, Malho R. 1997. Signal perception and transduction: Theorigin of the phenotype. The Plant Cell 9: 1181±1195.

Venis MA, Napier RM, Olivier S. 1996. Molecular analysis of auxin-speci®c signal transduction. Plant Growth Regulation 18: 1±6.

Ward JM, Schroeder JI. 1994. Calcium-activated K� channels andcalcium-induced calcium release by slow vacuolar channels inguard cell vacuoles implicated in the control of stomatal closure.The Plant Cell 6: 669±683.

Ward JM, Pei ZM, Schroeder JI. 1995. Roles of ion channels ininitiation of signal transduction in higher plants. The Plant Cell 7:833±844.

White PJ. 1997. Cation channels in the plasma membrane of rye roots.Journal of Experimental Botany 48: 499±514.

White PJ. 1998. Calcium channels in the plasma membrane of rootcells. Annals of Botany 81: 173±183.

White PJ. 1999. The molecular mechanism of sodium in¯ux to rootcells. Trends in Plant Science 4: 245±246.

White PJ, Biskup B, Elzenga JTM, Homann U, Thiel G, Wissing F,Maathuis FJM. 1999. Advanced patch-clamp techniques andsingle-channel analysis. Journal of Experimental Botany 50:1037±1054.

Willmott N, Sethi JK, Walseth TF, Lee HC, White AM, Galione A.1996. Nitric oxide-induced mobilization of intracellular calciumvia the cyclic ADP-ribose signalling pathway. The Journal ofBiological Chemistry 271: 3699±3705.

Wu W-H, Assmann SM. 1995. Is ATP required for K� channelsactivation in Vicia faba guard cells?. Plant Physiology 107:101±109.

Zimmermann S, Thomine S, Guern J, Barbier-Brygoo H. 1994. Ananion current at the plasma membrane of tobacco protoplastsshows ATP-dependent voltage regulation and is modulated byauxin. The Plant Journal 6: 707±716.

Zimmermann S, NuÈ rnberger T, Frachisse JM, Wirtz W, Guern J,Hedrich R, Scheel D. 1997. Receptor-mediated activation of aplant Ca2�-permeable ion channel involved in pathogen defense.Proceedings of the National Academy of Sciences, USA 94:


2751±2755.

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