A Suppressor Screen of the chimeric AtCNGC11/12 reveals residues important for intersubunit interactions of cyclic nucleotide-gated ion channels

Plant Physiology

Volumn 162, Issue 3, 2013, Pages 1681-1693

  Abdel Hamid, Huda ^a   Chin, Kimberley ^a   Moeder, Wolfgang ^a   Shahinas, Dea ^a   Gupta, Deepali ^a   Yoshioka, Keiko ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA BENTHAMIANA; SACCHAROMYCES CEREVISIAE;

EID: 84879736689     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.217539     Document Type: Article

References (50)

1. Abdel-Hamid H, Chin K, Shahinas D, Moeder W, Yoshioka K (2010) Calmodulin binding to Arabidopsis cyclic nucleotide gated ion channels. Plant Signal Behav 5: 1147-1149
2. Ali R, Zielinski RE, Berkowitz GA (2006) Expression of plant cyclic nucleotide-gated cation channels in yeast. J Exp Bot 57: 125-138
3. 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
4. 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
5. 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
6. Bradley J, Bönigk W, Yau KW, Frings S (2004) Calmodulin permanently associates with rat olfactory CNG channels under native conditions. Nat Neurosci 7: 705-710
7. Bridges D, Fraser ME, Moorhead GBG (2005) Cyclic nucleotide binding proteins in the Arabidopsis thaliana and Oryza sativa genomes. BMC Bioinformatics 6: 6
8. Chin K, Moeder W, Abdel-Hamid H, Shahinas D, Gupta D, Yoshioka K (2010) Importance of the alphaC-helix in the cyclic nucleotide binding domain for the stable channel regulation and function of cyclic nucleotide gated ion channels in Arabidopsis. J Exp Bot 61: 2383-2393
9. Chin K, Moeder W, Yoshioka K (2009) Biological roles of cyclic-nucleotidegated ion channels in plants: what we know and don't know about this 20 member ion channel family. Botany 87: 668-677
10. Craven KB, Zagotta WN (2004) Salt bridges and gating in the COOH-terminal region of HCN2 and CNGA1 channels. J Gen Physiol 124: 663-677
11. Cukkemane A, Seifert R, Kaupp UB (2011) Cooperative and uncooperative cyclic-nucleotide-gated ion channels. Trends Biochem Sci 36: 55-64
12. Daram P, Urbach S, Gaymard F, Sentenac H, Chérel I (1997) Tetramerization of the AKT1 plant potassium channel involves its C-terminal cytoplasmic domain. EMBO J 16: 3455-3463
13. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, Palo Alto, CA
14. Dietrich P, Anschütz U, Kugler A, Becker D (2010) Physiology and biophysics of plant ligand-gated ion channels. Plant Biol (Stuttg) (Suppl 1) 12: 80-93
15. Dreyer I, Antunes S, Hoshi T, Müller-Röber B, Palme K, Pongs O, Reintanz B, Hedrich R (1997) Plant K+ channel alpha-subunits assemble indiscriminately. Biophys J 72: 2143-2150
16. Dreyer I, Porée F, Schneider A, Mittelstädt J, Bertl A, Sentenac H, Thibaud JB, Mueller-Roeber B (2004) Assembly of plant Shaker-like K (out) channels requires two distinct sites of the channel alpha-subunit. Biophys J 87: 858-872
17. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616-629
18. Fesenko EE, Kolesnikov SS, Lyubarsky AL (1985) Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313: 310-313
19. Finka A, Cuendet AF, Maathuis FJ, Saidi Y, Goloubinoff P (2012) Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell 24: 3333-3348
20. Flynn GE, Black KD, Islas LD, Sankaran B, Zagotta WN (2007) Structure and rearrangements in the carboxy-terminal region of SpIH channels. Structure 15: 671-682
21. Holm L, Park J (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16: 566-567
22. 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
23. Kaplan B, Sherman T, Fromm H (2007) Cyclic nucleotide-gated channels in plants. FEBS Lett 581: 2237-2246
24. Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82: 769-824
25. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4: 363-371
26. 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
27. Köhler C, Neuhaus G (1998) Cloning and partial characterization of two putative cyclic nucleotide-regulated ion channels from Arabidopsis thaliana, designated CNGC1 (Y16327), CNGC2 (Y16328) (PGR98-062). Plant Physiol 116: 1604
28. 2+ regulates the sensitivity of cyclic nucleotide-gated channels in olfactory receptor neurons. Neuron 9: 897-906
29. 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
30. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126: 1646-1667
31. Moeder W, Urquhart W, Ung H, Yoshioka K (2011) The role of cyclic nucleotide-gated ion channels in plant immunity. Mol Plant 4: 442-452
32. Naso A, Dreyer I, Pedemonte L, Testa I, Gomez-Porras JL, Usai C, Mueller-Rueber B, Diaspro A, Gambale F, Picco C (2009) The role of the C-terminus for functional heteromerization of the plant channel KDC1. Biophys J 96: 4063-4074
33. Peng C, Rich ED, Varnum MD (2004) Subunit configuration of heteromeric cone cyclic nucleotide-gated channels. Neuron 42: 401-410
34. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65: 453-480
35. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res 33: W363-W367
36. 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
37. Silva H, Yoshioka K, Dooner HK, Klessig DF (1999) Characterization of a new Arabidopsis mutant exhibiting enhanced disease resistance. Mol Plant Microbe Interact 12: 1053-1063
38. 2+/CaM via the B1b subunit affects response termination but not sensitivity to recurring stimulation. Neuron 58: 374-386
39. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234
40. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680
41. Ungerer N, Mücke N, Broecker J, Keller S, Frings S, Möhrlen F (2011) Distinct binding properties distinguish LQ-type calmodulin-binding domains in cyclic nucleotide-gated channels. Biochemistry 50: 3221-3228
42. Urbach S, Chérel I, Sentenac H, Gaymard F (2000) Biochemical characterization of the Arabidopsis K+ channels KAT1 and AKT1 expressed or co-expressed in insect cells. Plant J 23: 527-538
43. 2+ dependent manner. Plant Mol Biol 65: 747-761
44. Wissinger B, Gamer D, Jägle H, Giorda R, Marx T, Mayer S, Tippmann S, Broghammer M, Jurklies B, Rosenberg T, et al (2001) CNGA3 mutations in hereditary cone photoreceptor disorders. Am J Hum Genet 69: 722-737
45. Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J, Klessig DF (2001) Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. Plant J 26: 447-459
46. Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K, Berkowitz G, Klessig DF (2006) The chimeric Arabidopsis CYCLIC NUCLEOTIDEGATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18: 747-763
47. Zagotta WN, Olivier NB, Black KD, Young EC, Olson R, Gouaux E (2003) Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425: 200-205
48. Zagotta WN, Siegelbaum SA (1996) Structure and function of cyclic nucleotide-gated channels. Annu Rev Neurosci 19: 235-263
49. Zhong H, Molday LL, Molday RS, Yau KW (2002) The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature 420: 193-198
50. + channel SKT1 is co-expressed with KST1 in potato guard cells: both channels can co-assemble via their conserved KT domains. Plant J 28: 517-527