Roles of Ca2+ and cyclic nucleotide gated channel in plant innate immunity

Plant Science

Volumn 181, Issue 4, 2011, Pages 342-346

  Ma, Wei ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis; Calcium; Cyclic nucleotide gated channel; Nitric oxide; Plant innate immunity; Signal transduction

Indexed keywords

CALCIUM; CYCLIC NUCLEOTIDE GATED CHANNEL;

IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PLANT CELL; PLANT IMMUNITY; REVIEW; SIGNAL TRANSDUCTION;

CALCIUM; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; IMMUNITY, INNATE; PLANT CELLS; PLANT IMMUNITY; SIGNAL TRANSDUCTION;

ARABIDOPSIS;

EID: 80052315252     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2011.06.002     Document Type: Review

References (86)

1. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
2. Dangl J.L., Dietrich R.A., Richberg M.H. Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 1996, 8:1793-1807.
3. Torres M.A., Jones J.D., Dangl J.L. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 2006, 141:373-378.
4. Bouche N., Yellin A., Snedden W.A., Fromm H. Plant-specific calmodulin-binding proteins. Annu. Rev. Plant Biol. 2005, 56:435-466.
5. Demidchik V., Maathuis F.J. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol. 2007, 175:387-404.
6. Dodd A.N., Kudla J., Sanders D. The language of calcium signaling. Annu. Rev. Plant Biol. 2010, 61:593-620.
7. Hetherington A.M., Brownlee C. The generation of Ca2+ signals in plants. Annu. Rev. Plant Biol. 2004, 55:401-427.
8. McAinsh M.R., Pittman J.K. Shaping the calcium signature. New Phytol. 2009, 181:275-294.
9. Sanders D., Pelloux J., Brownlee C., Harper J.F. Calcium at the crossroads of signaling. Plant Cell 2002, 14(Suppl.):S401-417.
10. Ward J.M., Maser P., Schroeder J.I. Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 2009, 71:59-82.
11. Wheeler G.L, Brownlee C. Ca2+ signalling in plants and green algae-changing channels. Trends Plant Sci. 2008, 13:506-514.
12. Chin K., Moeder W., Yoshioka K. Biological roles of cyclic-nucleotide-gated ion channels in plants: what we know and don't know about this 20 member ion channel family. Botany 2009, 87:668-677.
13. Kaplan B., Sherman T., Fromm H. Cyclic nucleotide-gated channels in plants. FEBS Lett. 2007, 581:2237-2246.
14. Martinez-Atienza J., Van Ingelgem C., Roef L., Maathuis F.J. Plant cyclic nucleotide signalling: facts and fiction. Plant Signal. Behav. 2007, 2:540-543.
15. Moeder W., Urquhart W., Ung H., Yoshioka K. The role of cyclic nucleotide-gated ion channels in plant immunity. Mol. Plant 2011, 4:442-452.
16. Sherman T., Fromm H. Physiological roles of cyclic nucleotide gated channels in plants. Signaling in Plants, Signaling and Communication in Plants 2009, 91-106. Springer-Verlag, Berlin Heidelberg. F. Baluška, S. Mancuso (Eds.).
17. Talke I.N., Blaudez D., Maathuis F.J., Sanders D. CNGCs: prime targets of plant cyclic nucleotide signalling?. Trends Plant Sci. 2003, 8:286-293.
18. Garcia-Brugger A., Lamotte O., Vandelle E., Bourque S., Lecourieux D., Poinssot B., Wendehenne D., Pugin A. Early signaling events induced by elicitors of plant defenses. Mol. Plant Microbe Interact. 2006, 19:711-724.
19. Lecourieux D., Ranjeva R., Pugin A. Calcium in plant defence-signalling pathways. New Phytol. 2006, 171:249-269.
20. Ma W., Berkowitz G.A. The grateful dead: calcium and cell death in plant innate immunity. Cell. Microbiol. 2007, 9:2571-2585.
21. Bent A.F., Mackey D. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 2007, 45:399-436.
22. Hofius D., Tsitsigiannis D.I., Jones J.D., Mundy J. Inducible cell death in plant immunity. Semin. Cancer Biol. 2007, 17:166-187.
23. Besson-Bard A., Pugin A., Wendehenne D. New insights into nitric oxide signaling in plants. Annu. Rev. Plant Biol. 2008, 59:21-39.
24. Courtois C., Besson A., Dahan J., Bourque S., Dobrowolska G., Pugin A., Wendehenne D. Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J. Exp. Bot. 2008, 59:155-163.
25. Delledonne M. NO news is good news for plants. Curr. Opin. Plant Biol. 2005, 8:390-396.
26. Leitner M., Vandelle E., Gaupels F., Bellin D., Delledonne M. NO signals in the haze: nitric oxide signalling in plant defence. Curr. Opin. Plant Biol. 2009, 12:451-458.
27. Ali R., Zielinski R.E., Berkowitz G.A. Expression of plant cyclic nucleotide-gated cation channels in yeast. J. Exp. Bot. 2006, 57:125-138.
28. Urquhart W., Gunawardena A.H., Moeder W., Ali R., Berkowitz G.A., Yoshioka K. The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner. Plant Mol. Biol. 2007, 65:747-761.
29. Frietsch S., Wang Y.F., Sladek C., Poulsen L.R., Romanowsky S.M., Schroeder J.I., Harper J.F. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc. Natl. Acad. Sci. USA 2007, 104:14531-14536.
30. Leng Q., Mercier R.W., Yao W., Berkowitz G.A. Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol. 1999, 121:753-761.
31. Lemtiri-Chlieh F., Berkowitz G.A. Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. J. Biol. Chem. 2004, 279:35306-35312.
32. Ali R., Ma W., Lemtiri-Chlieh F., Tsaltas D., Leng Q., von Bodman S., Berkowitz G.A. Death don't have no mercy and neither does calcium: Arabidopsis cyclic nucleotide gated channel2 and innate immunity. Plant Cell 2007, 19:1081-1095.
33. Ma W., Qi Z., Smigel A., Walker R.K., Verma R., Berkowitz G.A. Ca2+, cAMP, and transduction of non-self perception during plant immune responses. Proc. Natl. Acad. Sci. USA 2009, 106:20995-21000.
34. Qi Z., Verma R., Gehring C., Yamaguchi Y., Zhao Y., Ryan C.A., Berkowitz G.A. Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. Proc. Natl. Acad. Sci. USA 2010, 107:21193-21198.
35. Ma W., Smigel A., Walker R.K., Moeder W., Yoshioka K., Berkowitz G.A. Leaf senescence signaling: the Ca2+-conducting Arabidopsis cyclic nucleotide gated channel2 acts through nitric oxide to repress senescence programming. Plant Physiol. 2010, 154:733-743.
36. Balague C., Lin B., Alcon C., Flottes G., Malmstrom S., Kohler C., Neuhaus G., Pelletier G., Gaymard F., Roby D. HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 2003, 15:365-379.
37. Clough S.J., Fengler K.A., Yu I.C., Lippok B., Smith R.K., Bent A.F. The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl. Acad. Sci. USA 2000, 97:9323-9328.
38. Jurkowski G.I., Smith R.K., Yu I.C., Ham J.H., Sharma S.B., Klessig D.F., Fengler K.A., Bent A.F. Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the "defense, no death" phenotype. Mol. Plant Microbe Interact. 2004, 17:511-520.
39. Dangl J. Innate immunity. Plants just say NO to pathogens. Nature 1998, 394:525-527.
40. Grant M., Brown I., Adams S., Knight M., Ainslie A., Mansfield J. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J. 2000, 23:441-450.
41. Bolwell G.P. A role for phosphorylation in the down-regulation of phenylalanine ammonia-lyase in suspension-cultured cells of French bean. Phytochemistry 1992, 31:4081-4086.
42. Cooke C.J., Smith C.J., Walton T.J., Newton R.P. Evidence that cyclic-AMP is involved in the hypersensitive response of Medicago sativa to a fungal elicitor. Phytochemistry 1994, 35:889-895.
43. Kurosaki F., Tsurusawa Y., Nishi A. The elicitation of phytoalexins by Ca2+ and cyclic AMP in carrot cells. Phytochemistry 1987, 26:1919-1923.
44. Bindschedler L.V., Minibayeva F., Gardner S.L., Gerrish C., Davies D.R., Bolwell G.P. Early signalling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+. New Phytol. 2001, 151:185-194.
45. Jeworutzki E., Roelfsema M.R., Anschutz U., Krol E., Elzenga J.T., Felix G., Boller T., Hedrich R., Becker D. Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca-associated opening of plasma membrane anion channels. Plant J. 2010, 62:367-378.
46. Kwezi L., Meier S., Mungur L., Ruzvidzo O., Irving H., Gehring C. The Arabidopsis thaliana brassinosteroid receptor (AtBRI1) contains a domain that functions as a guanylyl cyclase in vitro. PLoS ONE 2007, 2:e449.
47. Boon E.M., Huang S.H., Marletta M.A. A molecular basis for NO selectivity in soluble guanylate cyclase. Nat. Chem. Biol. 2005, 1:53-59.
48. Durner J., Wendehenne D., Klessig D.F. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 1998, 95:10328-10333.
49. Isner J.C., Maathuis F.J. Measurement of cellular cGMP in plant cells and tissues using the endogenous fluorescent reporter FlincG. Plant J. 2011, 65:329-334.
50. Suita K., Kiryu T., Sawada M., Mitsui M., Nakagawa M., Kanamaru K., Yamagata H. Cyclic GMP acts as a common regulator for the transcriptional activation of the flavonoid biosynthetic pathway in soybean. Planta 2009, 229:403-413.
51. Huffaker A., Pearce G., Ryan C.A. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. USA 2006, 103:10098-10103.
52. Yamaguchi Y., Pearce G., Ryan C.A. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc. Natl. Acad. Sci. USA 2006, 103:10104-10109.
53. Ma W., Smigel A., Tsai Y.C., Braam J., Berkowitz G.A. Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol. 2008, 148:818-828.
54. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 2001, 357:593-615.
55. Stuehr D.J. Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1999, 1411:217-230.
56. Corpas F.J., Barroso J.B., Carreras A., Quiros M., Leon A.M., Romero-Puertas M.C., Esteban F.J., Valderrama R., Palma J.M., Sandalio L.M., Gomez M., del Rio L.A. Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol. 2004, 136:2722-2733.
57. Corpas F.J., Palma J.M., del Rio L.A., Barroso J.B. Evidence supporting the existence of L-arginine-dependent nitric oxide synthase activity in plants. New Phytol. 2009, 184:9-14.
58. del Rio L.A., Corpas F.J., Barroso J.B. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 2004, 65:783-792.
59. Delledonne M., Xia Y., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature 1998, 394:585-588.
60. Valderrama R., Corpas F.J., Carreras A., Fernandez-Ocana A., Chaki M., Luque F., Gomez-Rodriguez M.V., Colmenero-Varea P., Del Rio L.A., Barroso J.B. Nitrosative stress in plants. FEBS Lett. 2007, 581:453-461.
61. G.M., Crawford N.M., Tischner R., Heimer Y.M., Okamoto M.F Y.M., Mack A. Response to Zemojtel et al plant nitric oxide synthase back to square one. Trends Plant Sci. 2006, 11:524-525.
62. Guo F.Q., Okamoto M., Crawford N.M. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 2003, 302:100-103.
63. Zemojtel T., Frohlich A., Palmieri M.C., Kolanczyk M., Mikula I., Wyrwicz L.S., Wanker E.E., Mundlos S., Vingron M., Martasek P., Durner J. Plant nitric oxide synthase: a never-ending story?. Trends Plant Sci. 2006, 11:524-525. author reply 526-528.
64. Moreau M., Lee G.I., Wang Y., Crane B.R., Klessig D.F. AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J. Biol. Chem. 2008, 283:32957-32967.
65. Foresi N., Correa-Aragunde N., Parisi G., Calo G., Salerno G., Lamattina L. Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 2010, 22:3816-3830.
66. Heo W.D., Lee S.H., Kim M.C., Kim J.C., Chung W.S., Chun H.J., Lee K.J., Park C.Y., Park H.C., Choi J.Y., Cho M.J. Involvement of specific calmodulin isoforms in salicylic acid-independent activation of plant disease resistance responses. Proc. Natl. Acad. Sci. USA 1999, 96:766-771.
67. Chiasson D., Ekengren S.K., Martin G.B., Dobney S.L., Snedden W.A. Calmodulin-like proteins from Arabidopsis and tomato are involved in host defense against Pseudomonas syringae pv. tomato. Plant Mol. Biol. 2005, 58:887-897.
68. Takabatake R., Karita E., Seo S., Mitsuhara I., Kuchitsu K., Ohashi Y. Pathogen-induced calmodulin isoforms in basal resistance against bacterial and fungal pathogens in tobacco. Plant Cell Physiol. 2007, 48:414-423.
69. Harding S.A., Roberts D.M. Incompatible pathogen infection results in enhanced reactive oxygen and cell death responses in transgenic tobacco expressing a hyperactive mutant calmodulin. Planta 1998, 206:253-258.
70. Hua B.G., Mercier R.W., Zielinski R.E., Berkowitz G.A. Functional interaction of calmodulin with a plant cyclic nucleotide gated cation channels. Plant Physiol. Biochem. 2003, 41:945-954.
71. Li X.L., Borsics T., Harrington H.M., Christopher D.A. 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. 2005, 32:643-653.
72. Errakhi R., Dauphin A., Meimoun P., Lehner A., Reboutier D., Vatsa P., Briand J., Madiona K., Rona J.P., Barakate M., Wendehenne D., Beaulieu C., Bouteau F. An early Ca2+ influx is a prerequisite to thaxtomin A-induced cell death in Arabidopsis thaliana cells. J. Exp. Bot. 2008, 59:4259-4270.
73. Romeis T., Ludwig A.A., Martin R., Jones J.D. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 2001, 20:5556-5567.
74. Kobayashi M., Ohura I., Kawakita K., Yokota N., Fujiwara M., Shimamoto K., Doke N., Yoshioka H. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 2007, 19:1065-1080.
75. Sagi M., Fluhr R. Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 2001, 126:1281-1290.
76. Boudsocq M., Willmann M.R., McCormack M., Lee H., Shan L., He P., Bush J., Cheng S.H., Sheen J. Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 2010, 464:418-422.
77. Wang L., Tsuda K., Sato M., Cohen J.D., Katagiri F., Glazebrook J. Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog. 2009, 5:e1000301.
78. Galon Y., Nave R., Boyce J.M., Nachmias D., Knight M.R., Fromm H. Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett. 2008, 582:943-948.
79. Du L., Ali G.S., Simons K.A., Hou J., Yang T., Reddy A.S., Poovaiah B.W. Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 2009, 457:1154-1158.
80. Lamotte O., Gould K., Lecourieux D., Sequeira-Legrand A., Lebrun-Garcia A., Durner J., Pugin A., Wendehenne D. Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol. 2004, 135:516-529.
81. Vandelle E., Poinssot B., Wendehenne D., Bentejac M., Alain P. Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Mol. Plant Microbe Interact. 2006, 19:429-440.
82. Meier S., Madeo L., Ederli L., Donaldson L., Pasqualini S., Gehring C. Deciphering cGMP signatures and cGMP-dependent pathways in plant defence. Plant Signal. Behav. 2009, 4:307-309.
83. Klessig D.F., Durner J., Noad R., Navarre D.A., Wendehenne D., Kumar D., Zhou J.M., Shah J., Zhang S., Kachroo P., Trifa Y., Pontier D., Lam E., Silva H. Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. USA 2000, 97:8849-8855.
84. Zhu X., Caplan J., Mamillapalli P., Czymmek K., Dinesh-Kumar S.P. Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death. EMBO J. 2010, 29:1007-1018.
85. Boursiac Y., Lee S.M., Romanowsky S., Blank R., Sladek C., Chung W.S., Harper J.F. Disruption of the vacuolar calcium-ATPases in Arabidopsis results in the activation of a salicylic acid-dependent programmed cell death pathway. Plant Physiol. 2010, 154:1158-1171.
86. Zheng J., Zagotta W.N. Stoichiometry and assembly of olfactory cyclic nucleotide-gated channels. Neuron 2004, 42:411-421.