Signaling in cells and organisms - calcium holds the line

Current Opinion in Plant Biology

Volumn 22, Issue , 2014, Pages 14-21

  Steinhorst, Leonie ^a   Kudla, Jörg ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; REACTIVE OXYGEN METABOLITE;

METABOLISM; PHYSIOLOGY; SECOND MESSENGER; SIGNAL TRANSDUCTION;

CALCIUM; REACTIVE OXYGEN SPECIES; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

EID: 84907555812     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.08.003     Document Type: Review

References (83)

1. Rudd J.J., Franklin-Tong V.E. Calcium signaling in plants. Cell Mol Life Sci 1999, 55:214-232.
2. Sanders D., Brownlee C., Harper J.F. Communicating with calcium. Plant Cell 1999, 11:691-706.
3. Knight H., Knight M.R. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 2001, 6:262-267.
4. Sanders D., Pelloux J., Brownlee C., Harper J.F. Calcium at the crossroads of signaling. Plant Cell 2002, 14(Suppl.):S401-S417.
5. Scrase-Field S.A., Knight M.R. Calcium: just a chemical switch?. Curr Opin Plant Biol 2003, 6:500-506.
6. Berridge M.J. Unlocking the secrets of cell signaling. Annu Rev Physiol 2005, 67:1-21.
7. Clapham D.E. Calcium signaling. Cell 2007, 131:1047-1058.
8. Webb A.A., McAinsh M.R., Taylor J.E., Hetherington A.M. Calcium ions as intracellular second messengers in higher plants. Adv Bot Res 1996, 22:45-96.
9. Dodd A.N., Kudla J., Sanders D. The language of calcium signaling. Annu Rev Plant Biol 2010, 61:593-620.
10. Bush D.S. Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 1995, 46:95-122.
11. 2+ signalling in plants and green algae--changing channels. Trends Plant Sci 2008, 13:506-514.
12. Steinhorst L., Kudla J. Calcium and reactive oxygen species rule the waves of signaling. Plant Physiol 2013, 163:471-485.
13. 2+ signals through plant protein kinases. Annu Rev Plant Biol 2004, 55:263-288.
14. Batistič O., Kudla J. Calcium: not just another ion. Cell Biology of Metals and Nutrients 2010, 17-54. Springer-Verlag. R. Hell, R.R. Mendel (Eds.).
15. 2+-decoding signaling network: function and perspectives. New Phytol 2009, 184:517-528.
16. Dubiella U., Seybold H., Durian G., Komander E., Lassig R., Witte C.P., Schulze W.X., Romeis T. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A 2013, 110:8744-8749.
17. 2+ sensors CBL1 and CBL9 function in pollen germination and pollen tube growth in Arabidopsis. Mol Plant 2013, 6:1149-1162.
18. Gutermuth T., Lassig R., Portes M.T., Maierhofer T., Romeis T., Borst J.W., Hedrich R., Feijo J.A., Konrad K.R. Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 2013, 25:4525-4543.
19. Lassig R., Gutermuth T., Bey T.D., Konrad K.R., Romeis T. Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 2014, 78:94-106.
20. Matschi S., Werner S., Schulze W.X., Legen J., Hilger H.H., Romeis T. Function of calcium-dependent protein kinase CPK28 of Arabidopsis thaliana in plant stem elongation and vascular development. Plant J 2013, 73:883-896.
21. Romeis T., Herde M. From local to global: CDPKs in systemic defense signaling upon microbial and herbivore attack. Curr Opin Plant Biol 2014, 20C:1-10.
22. 2+-permeable channels and stomatal closure. PLoS Biol 2006, 4:e327.
23. 2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 2006, 48:857-872.
24. Cheong Y.H., Pandey G.K., Grant J.J., Batistič O., Li L., Kim B.G., Lee S.C., Kudla J., Luan S. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 2007, 52:223-239.
25. Franz S., Ehlert B., Liese A., Kurth J., Cazale A.C., Romeis T. Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant 2011, 4:83-96.
26. Drerup M.M., Schlücking K., Hashimoto K., Manishankar P., Steinhorst L., Kuchitsu K., Kudla J. The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 2013, 6:559-569.
27. Held K., Pascaud F., Eckert C., Gajdanowicz P., Hashimoto K., Corratge-Faillie C., Offenborn J.N., Lacombe B., Dreyer I., Thibaud J.B., Kudla J. Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 2011, 21:1116-1130.
28. Kudla J., Batistič O., Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell 2010, 22:541-563.
29. Geiger D., Maierhofer T., Al-Rasheid K.A., Scherzer S., Mumm P., Liese A., Ache P., Wellmann C., Marten I., Grill E., et al. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 2011, 4:ra32.
30. 2+ affinities. Proc Natl Acad Sci U S A 2010, 107:8023-8028.
31. Boudsocq M., Sheen J. CDPKs in immune and stress signaling. Trends Plant Sci 2013, 18:30-40.
32. 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.
33. Asai S., Ichikawa T., Nomura H., Kobayashi M., Kamiyoshihara Y., Mori H., Kadota Y., Zipfel C., Jones J.D., Yoshioka H. The variable domain of a plant calcium-dependent protein kinase (CDPK) confers subcellular localization and substrate recognition for NADPH oxidase. J Biol Chem 2013, 288:14332-14340.
34. Suzuki N., Mittler R. Reactive oxygen species-dependent wound responses in animals and plants. Free Radic Biol Med 2012, 53:2269-2276.
35. Suzuki N., Miller G., Salazar C., Mondal H.A., Shulaev E., Cortes D.F., Shuman J.L., Luo X., Shah J., Schlauch K., et al. Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 2013, 25:3553-3569.
36. Baxter A., Mittler R., Suzuki N. ROS as key players in plant stress signalling. J Exp Bot 2014, 65:1229-1240.
37. Mousavi S.A., Chauvin A., Pascaud F., Kellenberger S., Farmer E.E. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 2013, 500:422-426.
38. Nagata T., Iizumi S., Satoh K., Ooka H., Kawai J., Carninci P., Hayashizaki Y., Otomo Y., Murakami K., Matsubara K., Kikuchi S. Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Mol Biol Evol 2004, 21:1855-1870.
39. 2+ signaling systems. Trends Cell Biol 2011, 21:202-211.
40. 2+ signals in plants. Annu Rev Plant Biol 2004, 55:401-427.
41. Mäser P., Thomine S., Schroeder J.I., Ward J.M., Hirschi K., Sze H., Talke I.N., Amtmann A., Maathuis F.J., Sanders D., et al. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 2001, 126:1646-1667.
42. 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.
43. Ward J.M., Mäser P., Schroeder J.I. Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 2009, 71:59-82.
44. 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 U S A 2007, 104:14531-14536.
45. Chaiwongsar S., Strohm A.K., Roe J.R., Godiwalla R.Y., Chan C.W. A cyclic nucleotide-gated channel is necessary for optimum fertility in high-calcium environments. New Phytol 2009, 183:76-87.
46. 2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytol 2011, 190:566-572.
47. Tunc-Ozdemir M., Tang C., Ishka M.R., Brown E., Groves N.R., Myers C.T., Rato C., Poulsen L.R., McDowell S., Miller G., et al. A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 2013, 161:1010-1020.
48. Tunc-Ozdemir M., Rato C., Brown E., Rogers S., Mooneyham A., Frietsch S., Myers C.T., Poulsen L.R., Malho R., Harper J.F. Cyclic nucleotide gated channels 7 and 8 are essential for male reproductive fertility. PLOS ONE 2013, 8:e55277.
49. 2+-permeable channel. Mol Plant 2014, 7:739-743.
50. Zhou L., Lan W., Jiang Y., Fang W., Luan S. A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. Mol Plant 2014, 7:369-376.
51. Kim S.A., Kwak J.M., Jae S.K., Wang M.H., Nam H.G. Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol 2001, 42:74-84.
52. Kang J., Turano F.J. The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2003, 100:6872-6877.
53. Kang J., Mehta S., Turano F.J. The putative glutamate receptor 1.1 (AtGLR1.1) in Arabidopsis thaliana regulates abscisic acid biosynthesis and signaling to control development and water loss. Plant Cell Physiol 2004, 45:1380-1389.
54. Qi Z., Stephens N.R., Spalding E.P. Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol 2006, 142:963-971.
55. Stephens N.R., Qi Z., Spalding E.P. Glutamate receptor subtypes evidenced by differences in desensitization and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiol 2008, 146:529-538.
56. 2+-programmed stomatal closure. Plant J 2009, 58:437-449.
57. Price M.B., Jelesko J., Okumoto S. Glutamate receptor homologs in plants: functions and evolutionary origins. Front Plant Sci 2012, 3:235.
58. Vincill E.D., Clarin A.E., Molenda J.N., Spalding E.P. Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation in Arabidopsis. Plant Cell 2013, 25:1304-1313.
59. 2+ channels in pollen tubes and are regulated by pistil d-serine. Science 2011, 332:434-437.
60. 2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol 2012, 159:40-46.
61. Manzoor H., Kelloniemi J., Chiltz A., Wendehenne D., Pugin A., Poinssot B., Garcia-Brugger A. Involvement of the glutamate receptor AtGLR3.3 in plant defense signaling and resistance to Hyaloperonospora arabidopsidis. Plant J 2013, 76:466-480.
62. Li F., Wang J., Ma C., Zhao Y., Wang Y., Hasi A., Qi Z. Glutamate receptor-like channel3.3 is involved in mediating glutathione-triggered cytosolic calcium transients, transcriptional changes, and innate immunity responses in Arabidopsis. Plant Physiol 2013, 162:1497-1509.
63. 2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci U S A 2014, 111:6497-6502.
64. Knight M.R., Read N.D., Campbell A.K., Trewavas A.J. Imaging calcium dynamics in living plants using semi-synthetic recombinant aequorins. J Cell Biol 1993, 121:83-90.
65. Xiong T.C., Ronzier E., Sanchez F., Corratge-Faillie C., Mazars C., Thibaud J.B. Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter. Front Plant Sci 2014, 5:43.
66. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 2005, 434:404-408.
67. + channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 1994, 6:669-683.
68. 2+ release. Plant J 1997, 12:1387-1398.
69. Bewell M.A., Maathuis F.J., Allen G.J., Sanders D. Calcium-induced calcium release mediated by a voltage-activated cation channel in vacuolar vesicles from red beet. FEBS Lett 1999, 458:41-44.
70. Stephan A.B., Schroeder J.I. Plant salt stress status is transmitted systemically via propagating calcium waves. Proc Natl Acad Sci U S A 2014, 111:6126-6127.
71. Bonaventure G., Gfeller A., Proebsting W.M., Hortensteiner S., Chetelat A., Martinoia E., Farmer E.E. A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J 2007, 49:889-898.
72. Bonaventure G., Gfeller A., Rodriguez V.M., Armand F., Farmer E.E. The fou2 gain-of-function allele and the wild-type allele of Two Pore Channel 1 contribute to different extents or by different mechanisms to defense gene expression in Arabidopsis. Plant Cell Physiol 2007, 48:1775-1789.
73. Beyhl D., Hortensteiner S., Martinoia E., Farmer E.E., Fromm J., Marten I., Hedrich R. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J 2009, 58:715-723.
74. Mittler R., Vanderauwera S., Suzuki N., Miller G., Tognetti V.B., Vandepoele K., Gollery M., Shulaev V., Van Breusegem F. ROS signaling: the new wave?. Trends Plant Sci 2011, 16:300-309.
75. Wrzaczek M., Brosche M., Kangasjarvi J. ROS signaling loops - production, perception, regulation. Curr Opin Plant Biol 2013, 16:575-582.
76. Miller G., Schlauch K., Tam R., Cortes D., Torres M.A., Shulaev V., Dangl J.L., Mittler R. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2009, 2:ra45.
77. Kwak J.M., Mori I.C., Pei Z.M., Leonhardt N., Torres M.A., Dangl J.L., Bloom R.E., Bodde S., Jones J.D., Schroeder J.I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 2003, 22:2623-2633.
78. Torres M.A., Jones J.D., Dangl J.L. Pathogen-induced NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 2005, 37:1130-1134.
79. Torres M.A., Dangl J.L. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 2005, 8:397-403.
80. 2+ indicators. Science 2011, 333:1888-1891.
81. Belousov V.V., Fradkov A.F., Lukyanov K.A., Staroverov D.B., Shakhbazov K.S., Terskikh A.V., Lukyanov S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 2006, 3:281-286.
82. Matzke A.J., Matzke M. Membrane "potential-omics": toward voltage imaging at the cell population level in roots of living plants. Front Plant Sci 2013, 4:311.
83. Farmer E.E., Gasperini D., Acosta I.F. The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol 2014, 10.1111/nph.12897.