An IQ domain mediates the interaction with calmodulin in a plant cyclic nucleotide-gated channel

Plant and Cell Physiology

Volumn 54, Issue 4, 2013, Pages 573-584

  Fischer, Cornelia ^a   Kugler, Annette ^a,b   Hoth, Stefan ^a,c   Dietrich, Petra ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Arabidopsis; Calcium; Calmodulin; CNGC; IQ domain; Nuclear localization sequence

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM; CALMODULIN; CAM9 PROTEIN, ARABIDOPSIS; CYCLIC NUCLEOTIDE GATED CHANNEL;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; GENETICS; METABOLISM; PROTEIN BINDING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM; CALMODULIN; CELL MEMBRANE; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; PROTEIN BINDING;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 84875997593     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct021     Document Type: Article

References (63)

1. Abel, S., Savchenko, T. and Levy, M. (2005) Genome-wide comparative analysis of the IQD gene families in Arabidopsis thaliana and Oryza sativa. BMC Evol. Biol. 5: 72.
2. Arazi, T., Kaplan, B. and Fromm, H. (2000a) 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.
3. Arazi, T., Kaplan, B., Sunkar, R. and Fromm, H. (2000b) Cyclicnucleotide-and Ca2+/calmodulin-regulated channels in plants: targets for manipulating heavy-metal tolerance, and possible physiological roles. Biochem. Soc. Trans. 28: 471-475.
4. Ascencio-Ibanez, J.T., Sozzani, R., Lee, T.J., Chu, T.M., Wolfinger, R.D., Cella, R. et al. (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 148: 436-454.
5. Bähler, M. and Rhoads, A. (2002) Calmodulin signaling via the IQ motif. FEBS Lett. 513: 107-113.
6. Bouché, N., Yellin, A., Snedden, W.A. and Fromm, H. (2005) Plant-specific calmodulin-binding proteins. Annu. Rev. Plant Biol. 56: 435-466.
7. Buchan, D.W., Ward, S.M., Lobley, A.E., Nugent, T.C., Bryson, K. and Jones, D.T. (2010) Protein annotation and modelling servers at University College London. Nucleic Acids Res. 38: W563-W568.
8. Chan, C.W., Schorrak, L.M., Smith, R.K. Jr, Bent, A.F. and Sussman, M.R. (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plant development and adaptation to calcium stress. Plant Physiol. 132: 728-731.
9. Chin, K., Moeder, W. and Yoshioka, K. (2009) Biological roles of cyclicnucleotide-gated ion channels in plants: what we know and dont know about this 20 member ion channel family. Botany 87: 668-677.
10. Christopher, D.A., Borsics, T., Yuen, C.Y., Ullmer, W., Andeme-Ondzighi, C., Andres, M.A. et al. (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.
11. Clough, S.J., Fengler, K.A., Yu, I.C., Lippok, B., Smith, R.K. Jr and Bent, A.F. (2000) The Arabidopsis dnd1 defense, no death gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl Acad. Sci. USA 97: 9323-9328.
12. Cukkemane, A., Seifert, R. and Kaupp, U.B. (2011) Cooperative and uncooperative cyclic-nucleotide-gated ion channels. Trends Biochem. Sci. 36: 55-64.
13. Curtis, M.D. and Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462-469.
14. de Castro, E., Sigrist, C.J., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P.S., Gasteiger, E. et al. (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34: W362-W365.
15. DeFalco, T.A., Bender, K.W. and Snedden, W.A. (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem. J. 425: 27-40.
16. Dietrich, P., Anschütz, U., Kugler, A. and Becker, D. (2010) Physiology and biophysics of plant ligand-gated ion channels. Plant Biol. 12: 80-93.
17. Dodd, A.N., Kudla, J. and Sanders, D. (2010) The language of calcium signaling. Annu. Rev. Plant Biol. 61: 593-620.
18. Dunlap, K. (2007) Calcium channels are models of self-control. J. Gen. Physiol. 129: 379-383.
19. Etxeberria, A., Aivar, P., Rodriguez-Alfaro, J.A., Alaimo, A., Villace, P., Gomez-Posada, J.C. et al. (2008) Calmodulin regulates the trafficking of KCNQ2 potassium channels. FASEB J. 22: 1135-1143.
20. Finka, A., Cuendet, A.F., Maathuis, F.J., Saidi, Y. and Goloubinoff, P. (2012) Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell 24: 3333-3348.
21. Gautier, R., Douguet, D., Antonny, B. and Drin, G. (2008) HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics 24: 2101-2102.
22. Gawienowski, M.C., Szymanski, D., Perera, I.Y. and Zielinski, R.E. (1993) Calmodulin isoforms in Arabidopsis encoded by multiple divergent mRNAs. Plant Mol. Biol. 22: 215-225.
23. Gehl, C., Waadt, R., Kudla, J., Mendel, R.R. and Hansch, R. (2009) New GATEWAY vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation. Mol. Plant. 2: 1051-1058.
24. Gomez-Ospina, N., Tsuruta, F., Barreto-Chang, O., Hu, L. and Dolmetsch, R. (2006) The C terminus of the L-type voltage-gated calcium channel Ca(V)1. 2 encodes a transcription factor. Cell 127: 591-606.
25. Hammes, U.Z., Schachtman, D.P., Berg, R.H., Nielsen, E., Koch, W., McIntyre, L.M. et al. (2005) Nematode-induced changes of transporter gene expression in Arabidopsis roots. Mol. Plant-Microbe Interact. 18: 1247-1257.
26. Holmes, K.D., Mattar, P., Marsh, D.R., Jordan, V., Weaver, L.C. and Dekaban, G.A. (2002) The C-terminal C1 cassette of the N-methyl-D-aspartate receptor 1 subunit contains a bi-partite nuclear localization sequence. J. Neurochem. 81: 1152-1165.
27. Hua, B.G., Mercier, R.W., Zielinski, R.E. and Berkowitz, G. (2003) Functional interaction of calmodulin with a plant cyclic nucleotide gated cation channel. Plant Physiol. Biochem. 41: 945-954.
28. Kanter, U., Hauser, A., Michalke, B., Draxl, S. and Schaffner, A.R. (2010) Caesium and strontium accumulation in shoots of Arabidopsis thaliana: genetic and physiological aspects. J. Exp. Bot. 61: 3995-4009.
29. Kaplan, B., Sherman, T. and Fromm, H. (2007) Cyclic nucleotide-gated channels in plants. FEBS Lett. 581: 2237-2246.
30. Karimi, M., Inze, D. and Depicker, A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
31. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O. et al. (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50: 347-363.
32. Köhler, C. and Neuhaus, G. (2000) Characterisation of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana. FEBS Lett. 471: 133-136.
33. Kugler, A., Köhler, B., Wolff, P., Palme, K. and Dietrich, P. (2009) Salt-dependent regulation of a CNG channel subfamily in Arabidopsis. BMC Plant Biol. 9: 140-151.
34. Leba, L.J., Cheval, C., Ortiz-Martin, I., Ranty, B., Beuzon, C.R., Galaud, J.P. et al. (2012) CML9, an Arabidopsis calmodulin-like protein, contributes to plant innate immunity through a flagellin-dependent signalling pathway. Plant J. 71: 976-989.
35. Letunic, I., Doerks, T. and Bork, P. (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40: D302-D305.
36. Magnan, F., Ranty, B., Charpenteau, M., Sotta, B., Galaud, J.P. and 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.
37. Mäser, P., Thomine, S., Schroeder, J.I., Ward, J.M., Hirschi, K., Sze, H. et al. (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126: 1646-1667.
38. McCormack, E. and Braam, J. (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol. 159: 585-598.
39. McCormack, E., Tsai, Y.C. and Braam, J. (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci. 10: 383-389.
40. Melzer, N., Villmann, C., Becker, K., Harvey, K., Harvey, R.J., Vogel, N. et al. (2010) Multifunctional basic motif in the glycine receptor intracellular domain induces subunit-specific sorting. J. Biol. Chem. 285: 3730-3739.
41. Michelsen, K., Yuan, H. and Schwappach, B. (2005) Hide and run. Arginine-based endoplasmic-reticulum-sorting motifs in the assembly of heteromultimeric membrane proteins. EMBO Rep. 6: 717-722.
42. Mruk, K., Shandilya, S.M., Blaustein, R.O., Schiffer, C.A. and Kobertz, W.R. (2012) Structural insights into neuronal K+ channel-calmodulin complexes. Proc. Natl Acad. Sci. USA 109: 13579-13583.
43. ONeil, K.T. and DeGrado, W.F. (1990) How calmodulin binds its targets: sequence independent recognition of amphiphilic alpha-helices. Trends Biochem. Sci. 15: 59-64.
44. Pate, P., Mochca-Morales, J., Wu, Y., Zhang, J.Z., Rodney, G.G., Serysheva, I.I. et al. (2000) Determinants for calmodulin binding on voltage-dependent Ca2+ channels. J. Biol. Chem. 275: 39786-39792.
45. Perochon, A., Aldon, D., Galaud, J.P. and Ranty, B. (2011) Calmodulin and calmodulin-like proteins in plant calcium signaling. Biochimie 93: 2048-2053.
46. Peterson, B.Z., DeMaria, C.D., Adelman, J.P. and Yue, D.T. (1999) Calmodulin is the Ca2+ sensor for Ca2+-dependent inactivation of L-type calcium channels. Neuron 22: 549-558.
47. Pitt, G.S., Zuhlke, R.D., Hudmon, A., Schulman, H., Reuter, H. and Tsien, R.W. (2001) Molecular basis of calmodulin tethering and Ca2+-dependent inactivation of L-type Ca2+ channels. J. Biol. Chem. 276: 30794-30802.
48. Popescu, S.C., Popescu, G.V., Bachan, S., Zhang, Z., Seay, M., Gerstein, M. et al. (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.
49. Reddy, V.S., Ali, G.S. and Reddy, A.S. (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J. Biol. Chem. 277: 9840-9852.
50. Rhoads, A.R. and Friedberg, F. (1997) Sequence motifs for calmodulin recognition. FASEB J. 11: 331-340.
51. Rost, B., Yachdav, G. and Liu, J. (2004) The PredictProtein server. Nucleic Acids Res. 32: W321-W326.
52. Sanders, D., Pelloux, J., Brownlee, C. and Harper, J.F. (2002) Calcium at the crossroads of signaling. Plant Cell. 14(Suppl), S401-S417.
53. Schuurink, R.C., Shartzer, S.F., Fath, A. and Jones, R.L. (1998) Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone. Proc. Natl Acad. Sci. USA 95: 1944-1949.
54. Trudeau, M.C. and Zagotta, W.N. (2004) Dynamics of Ca2+-calmodulin- dependent inhibition of rod cyclic nucleotide-gated channels measured by patch-clamp fluorometry. J. Gen. Physiol. 124: 211-223.
55. Ungerer, N., Mücke, N., Broecker, J., Keller, S., Frings, S. and Möhrlen, F. (2011) Distinct binding properties distinguish LQ-type calmodulin-binding domains in cyclic nucleotide-gated channels. Biochemistry 50: 3221-3228.
56. Voinnet, O., Rivas, S., Mestre, P. and Baulcombe, D. (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
57. Walter, M., Chaban, C., Schutze, K., Batistic, O., Weckermann, K., Nake, C. et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
58. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V. and Provart, N.J. (2007) An Electronic Fluorescent Pictograph browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718.
59. Yamniuk, A.P. and Vogel, H.J. (2004) Calmodulins flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol. Biotechnol. 27: 33-57.
60. Yu, I., Fengler, K.A., Clough, S.J. and Bent, A.F. (2000) Identification of Arabidopsis mutants exhibiting an altered hypersensitive response in gene-for-gene disease resistance. Mol. Plant-Microbe Interact. 13: 277-286.
61. Zagotta, W.N., Olivier, N.B., Black, K.D., Young, E.C., Olson, R. and Gouaux, E. (2003) Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425: 200-205.
62. Zerangue, N., Malan, M.J., Fried, S.R., Dazin, P.F., Jan, Y.N., Jan, L.Y. et al. (2001) Analysis of endoplasmic reticulum trafficking signals by combinatorial screening in mammalian cells. Proc. Natl Acad. Sci. US. 98: 2431-2436.
63. Zühlke, R.D., Pitt, G.S., Tsien, R.W. and Reuter, H. (2000) Ca2+-sensitive inactivation and facilitation of L-type Ca2+ channels both depend on specific amino acid residues in a consensus calmodulinbinding motif in the (alpha)1C subunit. J. Biol. Chem. 275: 21121-21129.