Skip to main content
SpringerLink
Log in

The cyclic nucleotide-gated calmodulin-binding channel AtCNGC10 localizes to the plasma membrane and influences numerous growth responses and starch accumulation in Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Cyclic nucleotide gated channels (CNGCs) that are regulated by calmodulin (CaM) have been shown to play essential roles in signal transduction, metabolism, and growth in animals. By contrast, very little is known about the subcellular location and the function of these channels in plants. Here we report on the effects of antisense suppression of the expression of AtCNGC10, a putative K+ channel, and the immunolocalization of the protein using an AtCNGC10-specific antiserum. In Arabidopsis thaliana leaves, AtCNGC10 was localized to the plasma membrane of mesophyll and parenchyma cells. Antisense AtCNGC10 plants had 40% of the AtCNGC10 mRNA levels and virtually undetectable protein levels relative to wild type plants. Antisense expression of AtCNGC10 did not affect the mRNA levels of AtCNGC13, the most closely related CNGC family member in the genome. Relative to wild type Columbia, antisense AtCNGC10 plants flowered 10 days earlier, and had a 25% reduction in leaf surface area, thickness and palisade parenchyma cell length. Their roots responded more slowly to gravitropic changes and the chloroplasts accumulated more starch. We propose that AtCNGC10, through interactions with CaM and cGMP, modulates cellular K+ balance across the plasma membrane, and that perturbations of this K+ gradient affect numerous growth and developmental processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89:3736–3740

    Article  PubMed  CAS  Google Scholar 

  • Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plama membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20:171–182

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Blum DE, Elzenga TM, Linnemeyer PA, Van Volkenburgh E (1992) Stimulation of growth and ion uptake in bean leaves by red and blue light. Plant Physiol 100:1968–1975

    PubMed  CAS  Google Scholar 

  • Bowler C, Neuhaus G, Yamagata H, Chua NH (1994) Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77:73–81

    Article  PubMed  CAS  Google Scholar 

  • Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46:95–122

    Article  CAS  Google Scholar 

  • Cao Y, Ward JM, Kelly WB, Ichida AM, Gaber RF, Anderson JA, Uozumi N, Schroeder JI, Crawford NM (1995) Multiple genes, tissue specificity, and expression-dependent modulation contribute to the functional diversity of potassium channels in Arabidopsis thaliana. Plant Physiol 109:1093–1106

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chory J, Peto CA, Ashbaugh M, Saginich R, Pratt L, Ausubel F (1989) Different roles for phytochrome in etiolated and green plants deduced from characterization of Arabidopsis thaliana mutants. Plant Cell 1:867–880

    Article  PubMed  CAS  Google Scholar 

  • Chun L, Kawakami A, Christopher DA (2001) Phytochrome A mediates blue light and UV-A-dependent chloroplast gene transcription in green leaves. Plant Physiol 125:1957–1966

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–43

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Fengler KA, Lippok B, Smith RK, Yu IC, 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

    Article  PubMed  CAS  Google Scholar 

  • Elumalai RP, Nagpal P, Reed JW (2002) A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14:119–131

    Article  PubMed  CAS  Google Scholar 

  • Finn JT, Grunwald ME, Yau K-W (1996) Cyclic nucleotide-gated ion channels: an extended family with diverse functions. Annu Rev Physiol 58:395–426

    Article  PubMed  CAS  Google Scholar 

  • Finn JT, Krautwurst D, Schroeder JE, Chen T-Y, Reed RR, Yau K-W (1998) Functional co-assembly among subunits of cyclic-nucleotide-activated nonselective cation channels, and across species from nematode to human. Biophys J 74:1333–1345

    PubMed  CAS  Google Scholar 

  • Flügge U-I (2000) Metabolite transport across the chloroplast envelope of C3-plants. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism. Kluwar, Dordrecht, pp 137–152

    Google Scholar 

  • Fodde R, Smits R (2002) Enhanced: a matter of dosage. Science 298:761–763

    Article  PubMed  CAS  Google Scholar 

  • Fox TC, Guerinot ML (1998) Molecular biology of cation transport in plants. Annu Rev Plant Physiol Plant Mol Biol 49:669–696

    Article  PubMed  CAS  Google Scholar 

  • Fuchs I, Philippar K, Ljung K, Sandberg G, Hedrich R (2003) Blue light regulates an auxin-induced K+-channel gene in the maize coleoptile. Proc Natl Acad Sci USA 100:11795–11800

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Grunwald ME, Zhong H, Yau K-W (1999) Molecular determinants of the modulation of cyclic nucleotide-activated channels by calmodulin. Proc Natl Acad Sci USA 96:13444–13449

    Article  PubMed  CAS  Google Scholar 

  • Gunning BES, Steer MW (1975) Ultrastructure and the biology of plant cells. Edward Arnold Publishers, London, pp 115–117

    Google Scholar 

  • Hennegan KP, Danna KJ (1998) pBIN20: An improved vector for shape Agrobacterium-mediated transformation. Plant Mol Biol Rep 16:129–131

    Article  CAS  Google Scholar 

  • Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–920

    Article  PubMed  CAS  Google Scholar 

  • Hu G, Yalpani N, Briggs SP, Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095–1105

    Article  PubMed  CAS  Google Scholar 

  • Hua BG, Mercier RW, Zielinski RE, Berkowitz GA (2003) Functional interaction of calmodulin with a plant cyclic nucleotide gated cation channel. Plant Physiol Biochem 41:945–954

    Article  CAS  Google Scholar 

  • Ketchum KA, Slayman CW (1996) Isolation of an ion channel gene from Arabidopsis thaliana using the H5 signature sequence from voltage-dependent K+ channels. FEBS Lett 378:19–26

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660

    Article  PubMed  CAS  Google Scholar 

  • Köhler C, Merkle T, Neuhaus G (1999) Characterization of a novel gene family of putatitive cyclic nucleotide- and calmodulin-regulated ion channels in Arabidopsis thaliana. Plant J 18:97–104

    Article  PubMed  Google Scholar 

  • Köhler C, Neuhaus G (2000) Characterization of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana. FEBS Lett 4710:133–136

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Li X-L, 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

    Article  CAS  Google Scholar 

  • Lin C (2000) Plant blue-light receptors. Trend Plant Sci 5:337–342

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C, Doll M, Fietz HJ, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants of sun and shade leaves. Photosyn Res 2:115–141

    Article  CAS  Google Scholar 

  • Maathuis FJ, Ichida AM, Sanders D, Schroeder JI (1997) Roles of higher plant K+ channels. Plant Physiol 114:1141–1149

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, Boston

    Google Scholar 

  • Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships with cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  PubMed  Google Scholar 

  • Moshelion M, Becker D, Czempinski K, Mueller-Roeber B, Attali B, Hedrich R, Moran N (2002) Diurnal and circadian regulation of putative potassium channels in a leaf moving organ. Plant Physiol 128:634–642

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus G, Bowler C, Kern R, Chua NH (1993) Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73:937–952

    Article  PubMed  CAS  Google Scholar 

  • Otegui M, Staehelin LA (2000) Syncytial type cell plates: a novel kind of cell plate involved in endosperm cellularization in Arabidopsis thaliana. Plant Cell 12:933–947

    Article  PubMed  CAS  Google Scholar 

  • Pan X, Li Y, Stein L (2005) Site preferences of insertional mutagenesis agents in Arabidopsis. Plant Physiol 137:168–175

    Article  PubMed  CAS  Google Scholar 

  • Philippar K, Fuchs I, Lüthen H, Hoth S, Bauer C, Haga K, Thiel G, Ljung K, Sandberg G, Böttger M, Becker D, Hedrich R (1999) Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropism. Proc Natl Acad Sci, USA 96:2186–12191

    Article  Google Scholar 

  • Philippar K, Ivashikina N, Ache P, Christian M, Luthen H, Palme K, Hedrich R (2004) Auxin activates KAT1 and KAT2, two K+-channel genes expressed in seedlings of Arabidopsis thaliana. Plant J 37:815–827

    Article  PubMed  CAS  Google Scholar 

  • Pyke K, Lopez-Juez E (1999) Cellular differentiation and leaf morphogenesis in Arabidopsis. Crit Rev Plant Sci 18:527–546

    Article  Google Scholar 

  • Quail PH (1997) The phytochromes: a biochemical mechanism of signaling in sight? Bioessays 19:571–579

    Article  PubMed  CAS  Google Scholar 

  • Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658

    Article  PubMed  CAS  Google Scholar 

  • Schuurink RC, Shartzer SF, Fath A, Jones RL (1998) Characterization of a calmodulin-binding transporter from plasma membrane of barley aleurone. Proc Natl Acad Sci USA 95:1944–1949

    Article  PubMed  CAS  Google Scholar 

  • Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon JM, Gaymard F, Grignon C (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256:663–665

    Article  PubMed  CAS  Google Scholar 

  • Stahlberg R, Van Volkenburgh E (1999) The effect of light on membrane potential, apoplastic pH and cell expansion in leaves of Pisum sativum L. var. Argentum. Planta 208:188–195

    Article  CAS  Google Scholar 

  • Stiles KA, Van Volkenburgh E (2002) Light-regulated leaf expansion in two Populus species: dependence on developmentally controlled ion transport. J Exp Bot 53:1651–1657

    Article  PubMed  CAS  Google Scholar 

  • Stiles KA, McClintick A, Van Volkenburgh E (2003) A developmental gradient in the mechanism of K+ uptake during light-stimulated leaf growth in Nicotiana tabacum L. Planta 217:587–596

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN, Maathuis FJ, 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

    Article  PubMed  CAS  Google Scholar 

  • Talke IN, Blaudez D, Maathuis FJ, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293

    Article  PubMed  CAS  Google Scholar 

  • Trudeau MC, Zagotta WN (2002) Mechanism of calcium/calmodulin inhibition of rod cyclic nucleotide-gated channels. Proc Natl Acad Sci USA 99:8424–8429

    Article  PubMed  CAS  Google Scholar 

  • Varnum MD, Zagotta WN (1997) Interdomain interactions underlying activation of cyclic nucleotide-gated channels. Science 278:110–113

    Article  PubMed  CAS  Google Scholar 

  • Very AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54:575–603

    Article  PubMed  CAS  Google Scholar 

  • Veitia RA (2002) Exploring the etiology of haploinsufficiency. Bioessays 24:175–84

    Article  PubMed  CAS  Google Scholar 

  • Weston E, Thorogood K, Vinti G, Lopez-Juez E (2000) Light quantity controls leaf-cell and chloroplast development in Arabidopsis thaliana wild type and blue-light-perception mutants. Planta 211:807–815

    Article  PubMed  CAS  Google Scholar 

  • Yoshioka K, Moeder W, Kang H-G, 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

    Article  PubMed  CAS  Google Scholar 

  • Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by funds from the US Department of Energy grant no. DE-FG02-03ER15395 to DAC.

Author information

Authors and Affiliations

  1. Department of Molecular Biosciences and Bioengineering, University of Hawaii, 1955 East-West Road, Agsciences 218, Honolulu, HI, 96822, USA

    Tamás Borsics & David A. Christopher

  2. Department of Botany, University of Hawaii, 3190 Maile Way, Honolulu, HI, 96822, USA

    David Webb

  3. Molecular, Cellular and Developmental Biology, University of Colorado at Boulder, UCB 347, Boulder, CO, 80309-0347, USA

    Christine Andeme-Ondzighi & L. Andrew Staehelin

Authors
  1. Tamás Borsics
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Webb
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christine Andeme-Ondzighi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. Andrew Staehelin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David A. Christopher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David A. Christopher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borsics, T., Webb, D., Andeme-Ondzighi, C. et al. 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 (2007). https://doi.org/10.1007/s00425-006-0372-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0372-3

Keywords

Search

Navigation