Annals of Botany 86: 449±469, 2000 doi: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 A precise control of ion channel opening is essential for the physiological functioning of plant cells. This process is termed gating. Ion channel gating can be eected by ligand-binding, ¯uctuations in membrane potential, membrane stretch and light quality. Modern electrophysiological and molecular-biological techniques have enabled the characterization and classi®cation of many ion channels according to their gating phenomena. Indications are that gating mechanisms are complex and that individual ion channels can be regulated by a number of factors. In this paper, gating mechanisms are reviewed following a standard classi®cation of ion channels based on permeability. The gating of K,Ca2 and anion channels in the plasma membrane, tonoplast and endomembranes of plant cells is described. # 2000 Annals of Botany Company Key words: Review, ion channel, ligand-gating, voltage-gating, stretch-gating, light-gating, plasmalemma, tonoplast. INTRODUCTION are also involved in membrane voltage stabilization, which is critical for maintaining ionic gradients and nutritional Ion channels are integral components of all membranes and ion ¯uxes. Stretch-activated ion channels serve as addi- they can be viewed as dynamic ion transport systems tional speci®c transmembrane `receptors' co-existing with coupled via membrane electrical activities (White et al., other cellular volume-sensing mechanisms. Light-activated 1999). Not only do they in¯uence membrane voltage channels are in fact ligand-gated, although a precise through the ionic currents they mediate, but their activities indication of the ligands is not yet possible because the can also be regulated by membrane voltage. Ion channels process of light signal transduction remains unclear. These can be divided into four `historically-based' groups accord- channels are distinguished particularly because of a special ing to gating mechanism: ligand-gated, voltage-gated, importance of light stimuli in plant signalling processes. stretch-activated and light-activated. Ligand-gated ion Modern biomolecular techniques reveal how complicated channels bind intracellular second messengers which pro- the processes controlling channel behaviour are. It becomes vide the essential links between external stimuli and speci®c increasingly apparent that the activity of a channel may intracellular responses (Leckie et al., 1998). Moreover, depend on the developmental and metabolic stage of the additional modulations by ATP or protons make the cell. Moreover, regulation of ion channels relies not only on channels capable of sensing changes in energy status or the channel proteins themselves, but also to a great extent acid metabolism, respectively (Schulz-Lessdorf et al., 1996). on regulatory polypeptides, such as auxiliary b-subunits, Voltage-dependent channels appear optimally suited for cytoskeletal components, 14-3-3 proteins, phosphates, electrical signal transmission via membrane depolarization kinases, and G-proteins (Czempinski et al., 1999). (e.g. through action potentials) and/or for signal trans- Jan and Jan (1997) recently reviewed receptor-regulated duction in response to changes in membrane potential ion channels in excitable and nonexcitable animal tissues (e.g. models investigating the coupling between membrane (G-protein-gated and cGMP-gated K channels; voltage- potential and voltage-dependent Ca2-channels suggest gated K-, Na-, Cl-, Ca2 channels; voltage-insensitive that these are engaged in intracellular signalling). They Ca2 channels; Ca2-activated K channels; ligand-gated Ca2 channels). The activities of these channels are sensi- * For correspondence. E-mail [email protected] tive to external and internal signals that are mediated by Abbreviations: ABA, Abscisic acid; ABC, ATP binding cassette; receptors for hormones and transmitters. There are also A-9-C, anthracene-9-carboxylic acid; AP, action potential; BL, blue light; cADPR, cyclic ADP-ribose; CDPK, calmodulin-like domain plant-derived elicitor-speci®c receptors, which are closely protein kinase; DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethyl urea; E, coupled with plasma membrane ion channels important for equilibrium potential; I, current intensity; IAA, indol-3-acetic acid; IP3, signal transduction in plant cells (Ward et al., 1995; inositol triphosphate; NPPB, (5-nitro-2-3-phenylpropylamino) benzoic Blumwald et al., 1998). Studies on receptor-regulated ion acid; OA, okadaic acid; PLC, phospholipase C; PKA, protein kinase 2 channels suggest that they too are gated via G-proteins, dependent on cyclic AMP; PKC, protein kinase dependent on [Ca ]cyt and phospholipids; PKG, protein kinase dependent on cyclic GMP; either by direct protein-protein interaction or indirectly TMB-8, 8 (N,N diethylamino) octyl-3,4,5-trimethoxybenzoate. by kinase (PKA, PKG, PKC)/phosphatase cascades or 0305-7364/00/090449+21 $35.00/00 # 2000 Annals of Botany Company 450 Krol and TrebaczÐIon Channel Gating in Plant Cells 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 membrane Trebacz et al., 1994; Elzenga et al., 1995, 1997; Blom-Zandstra et al., 1997; SchoÈ nknecht et al., potential changes 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 2 second messenger binding (Ca ,IP3 , cGMP, cAMP). A Schroeder, 1989; Roberts and Tester, 1995; Hedrich and growing body of evidence indicates that G-proteins, second Dietrich, 1996; Logan et al., 1997; Maathuis et al., 1997; messengers and phosphorylation/dephosphorylation pro- Czempinski et al., 1999). cesses mediate various plant responses through ion channel and other transport system regulation (Table 1). Moreover, plant transmembrane receptors resembling Ligand-gated potassium channels receptor kinases of animal cells are involved in mediating a Ligand binding causes conformational changes in variety of cellular processes and responses to diverse channel proteins. It is a process of great importance, extracellular signals (Braun and Walker, 1996; Trewavas especially during signal transduction cascades when second and Malho, 1997). PCR, advanced homology-based clon- messengers synchronize the metabolism of the cell with ing and function-complementation techniques have already environmental conditions and enhance the input stimuli. led to identi®cation of more than 70 plant protein kinase There are many K channels aected by calcium ion genes (Stone and Walker, 1995). However, the precise binding (namely: plasmalemma Kout channels, KORC, function of speci®c protein kinases and phosphatases NORC, VK, FV, SVÐfor more information see below) in during plant growth and development has been elucidated plant cells (Katsuhara and Tazawa, 1992; Allen and in only a few cases (Stone and Walker, 1995). Sanders, 1996; Czempinski et al., 1997, 1999; Maathuis et al., 1997; Muir et al., 1997; Allen et al., 1998a). Besides Ca2,H ions, nucleotides, proteins and plant hormones POTASSIUM CHANNELS can serve as potassium channel ligands (see below). Their Ion transport across all biological membranes is highly attachment corresponds accordingly to changes in voltage selective and thus electrochemical potentials can be sensitivity of voltage-gated K channels. generated. The electrochemical potentials largely depend on the potassium ion gradient, so most of the potassium Voltage-gated potassium channels in the plasmalemma channels