Abstract
The plant cyclic nucleotide-gated channels (CNGCs) are a large family of ion channels that are regulated by both cyclic nucleotides (CNs) and calmodulin (CaM). CNGCs are generally permeable to a wide range of cations, including the essential macronutrients K+ and Ca2+, as well as potentially toxic cations such as Na+ or Pb2+. Several members of the CNGC family have been implicated in the uptake of cations and/or their subsequent distribution across plant organs. Others may participate in plant responses to salinity and abiotic stress by mediating Ca2+ signaling. Some CNGCs localize to the plasma membrane (PM) whereas others localize to intracellular membranes such as the tonoplast, and may therefore regulate the sequestration and release of cations among intracellular stores. It thus appears that plants have adapted certain CNGCs for specialized roles in maintaining cellular cation homeostasis.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- AKT:
-
Arabidopsis K+ transporter
- AtKC1:
-
Arabidopsis thaliana K+ channel 1
- AtNHX7:
-
A. thaliana Na+/H+ exchanger 7
- AtSOS1:
-
A. thaliana salt overly sensitive 1
- CaM:
-
Calmodulin
- CaMBD:
-
Calmodulin-binding domain
- CAMP:
-
3′,5′-Cyclic adenyl monophosphate
- CGMP:
-
3′,5′-Cyclic guanyl monophosphate
- CML:
-
CaM-like
- CN:
-
Cyclic nucleotide
- CNBD:
-
Cyclic nucleotide-binding domain
- CNGA:
-
Cyclic nucleotide-gated channel subunit type A
- CNGB:
-
Cyclic nucleotide-gated channel subunit type B
- CNGC:
-
Cyclic nucleotide-gated channel
- CNTE:
-
Cyclic nucleotide-dependent thioesterase
- DEPC:
-
Diethyl pyrocarbonate
- EAG:
-
Ether-a-go-go
- EGTA:
-
Ethylene glycol-bis(2-aminoethylether)-N,N,N′,N′-tetraacetic acid
- ER:
-
Endoplasmic reticulum
- GLR:
-
Glutamate receptor
- GORK:
-
Gated outwardly-rectifying K+ channel
- GUS:
-
β-Glucuronidase
- HACC:
-
Hyperpolarization-activated Ca2+ channel
- HCN:
-
Hyperpolarization-activated cyclic nucleotide-gated
- HEK:
-
Human embryonic kidney
- HvCBT1:
-
Hordeum vulgare calmodulin-binding transporter 1
- KAT:
-
K+ transporter of Arabidopsis thaliana
- KUP:
-
K+ uptake transporter
- MPSS:
-
Massively parallel signature sequencing
- NSCC:
-
Nonselective cation channel
- NtCBP4:
-
Nicotiana tabacum calmodulin-binding protein 4
- PM:
-
Plasma membrane
- ROS:
-
Reactive oxygen species
- SKOR:
-
Stelar K+ outward rectifier
- TPM:
-
Transcripts per million
- VI-NSCC:
-
Voltage-insensitive nonselective cation channel
References
Ali R, Zielinski RE, Berkowitz GA (2006) Expression of plant cyclic nucleotide-gated cation channels in yeast. J Exp Bot 57:125–138
Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA (2007) Death don’t have no mercy and neither does calcium: Arabidopsis cyclic nucleotide gated channel2 and innate immunity. Plant Cell 19:1081–1095
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20:171–182
Arazi T, Kaplan B, Fromm H (2000) A high-affinity calmodulin-binding site in a tobacco plasma-membrane channel protein coincides with a characteristic element of cyclic nucleotide-binding domains. Plant Mol Biol 42:591–601
Balagué C, Lin B, Alcon C, Flottes G, Malmström S, Köhler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365–379
Baxter J, Moeder W, Urquhart W, Shahinas D, Chin K, Christendat D, Kang HG, Angelova M, Kato N, Yoshioka K (2008) Identification of a functionally essential amino acid for Arabidopsis cyclic nucleotide gated ion channels using the chimeric AtCNGC11/12 gene. Plant J 56:457–469
Becker JD, Feijó JA (2007) How many genes are needed to make a pollen tube? Lessons from transcriptomics. Ann Bot 100:1117–1123
Borsics T, Webb D, Andeme-Ondzighi C, Staehelin LA, Christopher DA (2007) The cyclic nucleotide-gated calmodulin-binding channel AtCNGC10 localizes to the plasma membrane and influences numerous growth responses and starch accumulation in Arabidopsis thaliana. Planta 225:563–573
Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60:357–364
Bridges D, Fraser ME, Moorhead GB (2005) Cyclic nucleotide binding proteins in the Arabidopsis thaliana and Oryza sativa genomes. BMC Bioinformatics 6:6
Britto DT, Kronzucker HJ (2006) Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport. Trends Plant Sci 11:529–534
Broillet MC (2000) A single intracellular cysteine residue is responsible for the activation of the olfactory cyclic nucleotide-gated channel by NO. J Biol Chem 275:15135–15141
Chan CW, Schorrak LM, Smith RK Jr, Bent AF, Sussman MR (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plant development and adaptation to calcium stress. Plant Physiol 132:728–731
Chang F, Yan A, Zhao LN, Wu WH, Yang Z (2007) A putative calcium-permeable cyclic nucleotide-gated channel, CNGC18, regulates polarized pollen tube growth. J Integr Plant Biol 49:1261–1270
Christopher DA, Borsics T, Yuen CY, Ullmer W, Andème-Ondzighi C, Andres MA, Kang BH, Staehelin LA (2007) The cyclic nucleotide gated cation channel AtCNGC10 traffics from the ER via Golgi vesicles to the plasma membrane of Arabidopsis root and leaf cells. BMC Plant Biol 7:48
Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328
Davenport RJ, Tester M (2000) A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol 122:823–834
Delumeau O, Morère-le Paven MC, Montrichard F, Laval-Martin DL (2002) Effects of short-term NaCl stress on calmodulin transcript levels and calmodulin-dependent NAD kinase activity in two species of tomato. Plant Cell Environ 23:329–336
Demidchik V, Maathuis FJ (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404
Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387
Demidchik V, Bowen HC, Maathuis FJ, Shabala SN, Tester MA, White PJ, Davies JM (2002a) Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J 32:799–808
Demidchik V, Davenport RJ, Tester M (2002b) Nonselective cation channels in plants. Annu Rev Plant Biol 53:67–107
Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. J Cell Sci 116:81–88
Donaldson L, Ludidi N, Knight MR, Gehring C, Denby K (2004) Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels. FEBS Lett 569:317–320
Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77
Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333
Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci USA 49:684–692
Flowers TJ, Läuchli A (1983) Sodium versus potassium: substitution and compartmentation. In: Läuchli A, Bieleski RL (eds) Encyclopedia of plant physiology, new series, vol. 15B: Inorganic plant nutrition. Springer, Berlin, pp 651–681
Frietsch S, Wang YF, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104:14531–14536
Frings S (1999) Tuning Ca2+ permeation in cyclic nucleotide-gated channels. J Gen Physiol 113:795–798
Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100:11116–11121
Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJM (2006) Arabidopsis thaliana Cyclic Nucleotide Gated Channel 3 forms a non-selective ion transporter involved in germination and cation transport. J Exp Bot 57:791–800
Guo KM, Babourina O, Christopher DA, Borsics T, Rengel Z (2008) The cyclic nucleotide-gated channel, AtCNGC10, influences salt tolerance in Arabidopsis. Physiol Plant 134:499–507
Hampton CR, Bowen HC, Broadley MR, Hammond JP, Mead A, Payne KA, Pritchard J, White PJ (2004) Cesium toxicity in Arabidopsis. Plant Physiol 136:3824–3837
Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921
Hua BG, Mercier RW, Leng Q, Berkowitz GA (2003a) Plants do it differently. A new basis for potassium/sodium selectivity in the pore of an ion channel. Plant Physiol 132:1353–1361
Hua BG, Mercier RW, Zielinski RE, Berkowitz GA (2003b) Functional interaction of calmodulin with a plant cyclic nucleotide gated cation channel. Plant Physiol Biochem 41:945–954
Huang JW, Cunningham SD (1996) Lead phytoextraction: species variation in lead uptake and translocation. New Phytol 134: 75–84
Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82:769–824
Köhler C, Neuhaus G (2000) Characterisation of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana. FEBS Lett 471:133–136
Köhler C, Merkle T, Neuhaus G (1999) Characterisation of a novel gene family of putative cyclic nucleotide- and calmodulin-regulated ion channels in Arabidopsis thaliana. Plant J 18:97–104
Kurosaki F (1997) Stimulation of Ca2+-pumping ATPase activity in carrot plasma membrane by calmodulin. Phytochemistry 45:1097–1100
Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Annu Rev Plant Biol 54:109–136
Lau T-C, Stephenson AG (1994) Effects of soil phosphorus on pollen production, pollen size, pollen phosphorus content, and the ability to sire seeds in Cucurbita pepo (Cucurbitaceae). Sex Plant Reprod 7:215–220
Lee JS, Mulkey TJ, Evans ML (1983) Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol 73:874–876
Leitz G, Kang BH, Schoenwaelder ME, Staehelin LA (2009) Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. Plant Cell 21:843–860
Leng Q, Mercier RW, Yao W, Berkowitz GA (1999) Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol 121:753–761
Leng Q, Mercier RW, Hua BG, Fromm H, Berkowitz GA (2002) Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol 128:400–410
Li XL, Borsics T, Harrington HM, Christopher DA (2005) Arabidopsis AtCNGC10 rescues potassium channel mutants of E. coli, yeast and Arabidopsis and is regulated by calcium/calmodulin and cyclic GMP in E. coli. Funct Plant Biol 32:643–653
Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:897–903
Ma W, Ali R, Berkowitz GA (2006) Characterization of plant phenotypes associated with loss-of-function of AtCNGC1, a plant cyclic nucleotide gated cation channel. Plant Physiol Biochem 44:494–505
Maathuis FJ (2006) The role of monovalent cation transporters in plant responses to salinity. J Exp Bot 57:1137–1147
Maathuis FJ (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12:250–258
Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot (Lond) 84:123–133
Maathuis FJ, Sanders D (2001) Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol 127:1617–1625
Maathuis FJ, Filatov V, Herzyk P, Krijger GC, Axelsen KB, Chen S, Green BJ, Li Y, Madagan KL, Sánchez-Fernández R, Forde BG, Palmgren MG, Rea PA, Williams LE, Sanders D, Amtmann A (2003) Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J 35:675–692
Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D (2008) Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J 56:575–589
Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM, Sanders D, Harper JH, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667
McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytologist 159:585–598
McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389
Nebenführ A, Frohlick JA, Staehelin AL (2000) Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol 124:135–151
Newton RP, Smith CJ (2004) Cyclic nucleotides. Phytochemistry 65:2423–2437
Pilot G, Gaymard F, Mouline K, Chérel I, Sentenac H (2003a) Regulated expression of Arabidopsis shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol Biol 51:773–787
Pilot G, Pratelli R, Gaymard F, Meyer Y, Sentenac H (2003b) Five-group distribution of the Shaker-like K+ channel family in higher plants. J Mol Evol 56:418–434
Plieth C (2005) Calcium: Just another regulator in the machinery of life? Ann Bot (Lond) 96:1–8
Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci USA 104:4730–4735
Reddy VS, Ali GS, Reddy AS (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852
Schuurink RC, Shartzer SF, Fath A, Jones RL (1998) Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone. Proc Natl Acad Sci USA 95:1944–1949
Seifert R, Eismann E, Ludwig J, Baumann A, Kaupp UB (1999) Molecular determinants of a Ca2+-binding site in the pore of cyclic nucleotide-gated channels: S5/S6 segments control affinity of intrapore glutamates. EMBO J 18:119–130
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665
Snedden WA, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci 3:299–304
Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium: a functional plant nutrient. Crit Rev Plant Sci 22:391–416
Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN, Maathuis FJM, Sanders D, Bouchez D, Fromm H (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J 24:533–542
Talke IN, Blaudez D, Maathuis FJM, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293
Urquhart W, Gunawardena AH, Moeder W, Ali R, Berkowitz GA, Yoshioka K (2007) The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner. Plant Mol Biol 65:747–761
Véry AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci USA 97:9801–9806
Volotovski ID, Sokolovsky SG, Molchan OV, Knight MR (1998) Second messengers mediate increases in cytosolic calcium in tobacco protoplasts. Plant Physiol 117:1023–1030
White PJ, Broadley MR (2000) Mechanisms of cesium uptake by plants. New Phytol 147:241–256
White PJ, Broadley MR (2003) Calcium in plants. Ann Bot (Lond) 92:487–511
Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K, Berkowitz G, Klessig DF (2006) The chimeric Arabidopsis cyclic nucleotide-gated ion channel 11/12 activates multiple pathogen resistance responses. Plant Cell 18:747–763
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Yuen, C.Y.L., Christopher, D.A. (2010). The Role of Cyclic Nucleotide-Gated Channels in Cation Nutrition and Abiotic Stress. In: Demidchik, V., Maathuis, F. (eds) Ion Channels and Plant Stress Responses. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10494-7_7
Download citation
DOI: https://doi.org/10.1007/978-3-642-10494-7_7
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-10493-0
Online ISBN: 978-3-642-10494-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)