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  • Review Article
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Plants, symbiosis and parasites: a calcium signalling connection

Nature Reviews Molecular Cell Biology volume 6, pages 555–566 (2005)Cite this article

Key Points

  • CDPKs (calcium-dependent protein kinases) are defined by a unique structural arrangement in which the kinase domain is fused to a C-terminal calmodulin-like regulatory domain.

  • CDPKs are found in plants and some protists, such as the apicomplexan Plasmodium falciparum, a parasite that causes malaria in humans.

  • Structural studies on the mechanism of intra-molecular activation of a CDPK indicate that the N-terminal lobe of the calmodulin-like domain functions as the Ca2+ sensor that triggers activation.

  • CDPKs are targeted to many cellular locations, including the plasma membrane, endoplasmic reticulum, peroxisomes, nucleus and vacuoles. Localization of some isoforms is dynamic, as shown by stress signals that shift the localization of a plasma membrane CDPK to the nucleus.

  • An essential function for a CDPK has been shown in male gametogenesis in Plasmodium berghei. This validates CDPKs as a potential drug target against malaria and other apicomplexan-based diseases in humans and livestock.

  • A unique member of the CDPK-superfamily, CCaMK (chimeric Ca2+ and calmodulin-dependent protein kinase), decodes a Ca2+-oscillation signal in root hairs that are required for the initiation of bacterial and fungal (mycorrhizal) symbiosis. Symbiosis with a Rhizobium bacteria can result in nitrogen-fixing nodules in the roots of many legume plants. Symbiosis with mycorrhizae can result in improved nutrient acquisition from the soil for many important crop plants.

  • Conventional CDPKs have been implicated in the regulation of many aspects of plant biology, including pollen development, abiotic and biotic stress responses, hormone signalling, cytoskeleton regulation, proteosome regulation, carbon, nitrogen and sulphur metabolism, secondary metabolism and transcription.

Abstract

A unique family of protein kinases has evolved with regulatory domains containing sequences that are related to Ca2+-binding EF-hands. In this family, the archetypal Ca2+-dependent protein kinases (CDPKs) have been found in plants and some protists, including the malarial parasite, Plasmodium falciparum. Recent genetic evidence has revealed isoform-specific functions for a CDPK that is essential for Plasmodium berghei gametogenesis, and for a related chimeric Ca2+ and calmodulin-dependent protein kinase (CCaMK) that is essential to the formation of symbiotic nitrogen-fixing nodules in plants. In Arabidopsis thaliana, the analysis of 42 isoforms of CDPK and related kinases is expected to delineate Ca2+ signalling pathways in all aspects of plant biology.

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Figure 1: Structural differences between CDPK, CRK and CCaMK.
Figure 2: Activation of CDPK through intramolecular binding of the calmodulin-like domain.
Figure 3: The decoding of Ca2+ signals by CCaMK during the initiation of Rhizobium–Medicago truncatula symbiosis.
Figure 4: Biological functions of Ca2+-regulated protein kinases during the plant life cycle.

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References

  1. Clapham, D. E. Calcium signaling. Cell 80, 259–268 (1995).

    Article  CAS  PubMed  Google Scholar 

  2. Hetherington, A. M. & Brownlee, C. The generation of Ca2+ signals in plants. Annu. Rev. Plant Biol. 55, 401–427 (2004).

    Article  CAS  PubMed  Google Scholar 

  3. Sanders, D., Pelloux, J., Brownlee, C. & Harper, J. F. Calcium at the crossroads of signaling. Plant Cell 14 Supp., S401–417 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Taylor, L. P. & Hepler, P. K. Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 461–491 (1997).

    Article  CAS  PubMed  Google Scholar 

  5. Schiott, M. et al. A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc. Natl Acad. Sci. USA 101, 9502–9507 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Harper, J. F., Bretton, G. & Harmon, A. C. Decoding Ca2+ signals through plant protein kinases. Annu. Rev. Plant Biol. 55, 263–288 (2004). This review provides details about CDPKs and other Ca2+ regulated kinases that are not covered in this review.

    Article  CAS  PubMed  Google Scholar 

  7. Billker, O. et al. Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117, 503–514 (2004). This important paper provides genetic evidence for an essential function (the regulation of gametogenesis) of a CDPK.

    Article  CAS  PubMed  Google Scholar 

  8. Levy, J. et al. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364 (2004). This paper provides genetic evidence for an essential function of a plant Ca2+-regulated protein kinase in the initiation of bacterial and fungal symbioses.

    Article  CAS  PubMed  Google Scholar 

  9. Mitra, R. M. et al. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl Acad. Sci. USA 101, 4339–4340 (2004). This paper used an expression-profiling approach to identify a gene that encodes a CCaMK as crucial for the initiation of bacterial and fungal symbioses.

    Article  CAS  Google Scholar 

  10. Hrabak, E. M. et al. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132, 666–680 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cheng, S. H., Willmann, M. R., Chen, H. C. & Sheen, J. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 129, 469–485 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ludwig, A. A., Romeis, T. & Jones, J. D. G. CDPK-mediated signalling pathways: specificity and cross-talk. J. Exp. Botany 55, 181–188 (2004).

    Article  CAS  Google Scholar 

  13. Harper, J. F. et al. A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science 252, 951–954 (1991).

    Article  CAS  PubMed  Google Scholar 

  14. Suen, K. L. & Choi, J. H. Isolation and sequence analysis of a cDNA clone for a carrot calcium-dependent protein kinase: homology to calcium/calmodulin-dependent protein kinases and to calmodulin. Plant Mol. Biol. 17, 581–590 (1991).

    Article  CAS  PubMed  Google Scholar 

  15. Huang, J. F., Teyton, L. & Harper, J. F. Activation of a Ca2+-dependent protein kinase involves intramolecular binding of a calmodulin-like regulatory domain. Biochemistry 35, 13222–13230 (1996).

    Article  CAS  PubMed  Google Scholar 

  16. Harmon, A. C., Yoo, B. C. & McCaffery, C. Pseudosubstrate inhibition of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 33, 7278–7287 (1994).

    Article  CAS  PubMed  Google Scholar 

  17. Patil, S., Takezawa, D. & Poovaiah, B. W. Chimeric plant calcium/calmodulin-dependent protein-kinase gene with a neural visinin-like calcium-binding domain. Proc. Natl Acad. Sci. USA 92, 4897–4901 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hua, W., Li, R. J., Wang, L. & Lu, Y. T. A tobacco calmodulin-binding protein kinase (NtCBK2) induced by high-salt/GA treatment and its expression during floral development and embryogenesis. Plant Sci. 166, 1253–1259 (2004).

    Article  CAS  Google Scholar 

  19. Ma, L., Liang, S., Jones, R. L. & Lu, Y. T. Characterization of a novel calcium/calmodulin-dependent protein kinase from tobacco. Plant Physiol. 135, 1280–1293 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhang, L. & Lu, Y. T. Calmodulin-binding protein kinases in plants. Trends Plant Sci. 8, 123–127 (2003).

    Article  CAS  PubMed  Google Scholar 

  21. Furumoto, T., Ogawa, N., Hata, S. & Izui, K. Plant calcium-dependent protein kinase-related kinases (CRKs) do not require calcium for their activities. FEBS Lett. 396, 147–151 (1996).

    Article  CAS  PubMed  Google Scholar 

  22. Wang, Y., Liang, S., Xie, Q. G. & Lu, Y. T. Characterization of a calmodulin-regulated CDPK-related protein kinase, AtCRK1 from Arabidopsis. Biochem. J. 383, 73–81 (2004). This paper extends the observation that some CRKs are regulated by calmodulin to one of the eight CRKs of A. thaliana.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lindzen, E. & Choi, J. H. A carrot cDNA encoding an atypical protein kinase homologous to plant calcium-dependent protein kinases. Plant Mol. Biol. 28, 785–797 (1995).

    Article  CAS  PubMed  Google Scholar 

  24. Takezawa, D., Ramachandiran, S., V, P. & Poovaiah, B. Dual regulation of a chimeric plant serine/threonine kinase by calcium and calcium/calmodulin. J. Biol. Chem. 271, 8126–8132 (1996).

    Article  CAS  PubMed  Google Scholar 

  25. Christodoulou, J., Malmendal, A., Harper, J. F. & Chazin, W. J. Evidence for differing roles for each lobe of the calmodulin-like domain in a calcium-dependent protein kinase. J. Biol. Chem. 279, 29092–29100 (2004).

    Article  CAS  PubMed  Google Scholar 

  26. Weljie, A. M. & Vogel, H. J. Unexpected structure of the Ca2+-regulatory region from soybean calcium-dependent protein kinase-alpha. J. Biol. Chem. 279, 35494–35502 (2004).

    Article  CAS  PubMed  Google Scholar 

  27. Zhao, Y. et al. Calcium-binding properties of a calcium-dependent protein kinase from Plasmodium falciparum and the significance of individual calcium-binding sites for kinase activation. Biochemistry 33, 3714–3721 (1994).

    Article  CAS  PubMed  Google Scholar 

  28. Sathyanarayanan, P. V., Cremo, C. R. & Poovaiah, B. W. Plant chimeric Ca2+/calmodulin-dependent protein kinase. Role of the neural visinin-like domain in regulating autophosphorylation and calmodulin affinity. J. Biol. Chem. 275, 30417–30422 (2000). This paper demonstrates the unique regulatory properties of CCaMK.

    Article  CAS  PubMed  Google Scholar 

  29. Ward, P., Equinet, L., Packer, J. & Doerig, C. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5, 79 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Baxter, I. et al. Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol. 132, 618–628 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dammann, C. et al. Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol. 132, 1840–1848 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lu, S. X. & Hrabak, E. M. An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum. Plant Physiol. 128, 1008–1021 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Anil, V. S., Harmon, A. C. & Rao, K. S. Temporal association of Ca2+-dependent protein kinase with oil bodies during seed development in Santalum album L.: its biochemical characterization and significance. Plant Cell Physiol. 44, 367–376 (2003).

    Article  CAS  PubMed  Google Scholar 

  34. Pical, C., Fredlund, K. M., Petit, P. X., Sommarin, M. & Moller, I. M. The outer membrane of plant mitochondria contains a calcium-dependent protein kinase and multiple phosphoproteins. FEBS Lett. 336, 347–351 (1993).

    Article  CAS  PubMed  Google Scholar 

  35. Chehab, E. W., Patharkar, O. R., Hegeman, A. D., Taybi, T. & Cushman, J. C. Autophosphorylation and subcellular localization dynamics of a salt- and water deficit-induced calcium-dependent protein kinase from ice plant. Plant Physiol. 135, 1430–1446 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sheen, J. Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274, 1900–1902 (1996).

    Article  CAS  PubMed  Google Scholar 

  37. Huber, S. C. & Hardin, S. C. Numerous posttranslational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels. Curr. Opinion Plant Biol. 7, 318–322 (2004). An overview of the importance of post-translational modifications, including phosphorylation of proteins by CDPK, in regulating metabolic pathways in plants.

    Article  CAS  Google Scholar 

  38. Asano, T. et al. Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: phosphorylation of sucrose synthase is a possible factor. Plant Cell 14, 619–628 (2002). This paper shows the importance of CDPK for regulation of an agronomically important seed characteristic in rice.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Harmon, A. C., Gribskov, M. & Harper, J. F. CDPKs — a kinase for every Ca2+ signal? Trends Plant Sci. 5, 154–159 (2000).

    Article  CAS  PubMed  Google Scholar 

  40. Tatsuki, M. & Mori, H. Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the C-terminal region. J. Biol. Chem 276, 28051–28057 (2001).

    Article  CAS  PubMed  Google Scholar 

  41. Sebastia, C. H., Hardin, S. C., Clouse, S. D., Kieber, J. J. & Huber, S. C. Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch. Biochem. Biophys. 428, 81–89 (2004).

    Article  CAS  Google Scholar 

  42. Wang, K. L., Yoshida, H., Lurin, C. & Ecker, J. R. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428, 945–950 (2004).

    Article  CAS  PubMed  Google Scholar 

  43. Wang, W. & Poovaiah, B. W. Interaction of plant chimeric calcium/calmodulin-dependent protein kinase with a homolog of eukaryotic elongation factor-1-α. J. Biol. Chem. 274, 12001–12008 (1999).

    Article  CAS  PubMed  Google Scholar 

  44. Breman, J. G., Alilio, M. S. & Mills, A. Conquering the intolerable burden of malaria: what's new, what's needed: a summary. Am. J. Trop. Med. Hyg. 71, 1–15 (2004).

    Article  PubMed  Google Scholar 

  45. Le Roch, K. G. et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 1503–1508 (2003).

    Article  CAS  PubMed  Google Scholar 

  46. McCormick, S. Control of male gametophyte development. Plant Cell 16 Supp., S142–153 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Golovkin, M. & Reddy, A. S. A calmodulin-binding protein from Arabidopsis has an essential role in pollen germination. Proc. Natl Acad. Sci. USA 100, 10558–10563 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Estruch, J. J., Kadwell, S., Merlin, E. & Crossland, L. Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc. Natl Acad. Sci. USA 91, 8837–8841 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Poovaiah, B. W. et al. Developmental regulation of the gene for chimeric calcium/calmodulin-dependent protein kinase in anthers. Planta 209, 161–171 (1999).

    Article  CAS  PubMed  Google Scholar 

  50. Oldroyd, G. E. & Downie, J. A. Calcium, kinases and nodulation signalling in legumes. Nature Rev. Mol. Cell Biol. 5, 566–576 (2004).

    Article  CAS  Google Scholar 

  51. Ehrhardt, D. W., Wais, R. & Long, S. R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85, 673–681 (1996).

    Article  CAS  PubMed  Google Scholar 

  52. Ane, J. M. et al. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367 (2004).

    Article  CAS  PubMed  Google Scholar 

  53. Sathyanarayanan, P. V., Siems, W. F., Jones, J. P. & Poovaiah, B. W. Calcium-stimulated autophosphorylation site of plant chimeric calcium/calmodulin-dependent protein kinase. J. Biol. Chem. 276, 32940–32947 (2001).

    Article  CAS  PubMed  Google Scholar 

  54. Surpin, M. & Raikhel, N. Traffic jams affect plant development and signal transduction. Nature Rev. Mol. Cell Biol. 5, 100–109 (2004).

    Article  CAS  Google Scholar 

  55. McCubbin, A. G., Ritchie, S. M., Swanson, S. J. & Gilroy, S. The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar function. Plant J. 39, 206–218 (2004).

    Article  CAS  PubMed  Google Scholar 

  56. Gilroy, S. Signal transduction in barley aleurone protoplasts is calcium dependent and independent. Plant Cell 8, 2193–2209 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ritchie, S. & Gilroy, S. Calcium-dependent protein phosphorylation may mediate the gibberellic acid response in barley aleurone. Plant Physiol. 116, 765–776 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Nishi, T. & Forgac, M. The vacuolar H+-ATPases — nature's most versatile proton pumps. Nature Rev. Mol. Cell Biol. 3, 94–103 (2002).

    Article  CAS  Google Scholar 

  59. Desikan, R. et al. ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J. Exp. Bot. 55, 205–212 (2004).

    Article  CAS  PubMed  Google Scholar 

  60. Vitart, V., Christodoulou, J., Huang, J. F., Chazin, W. J. & Harper, J. F. Intramolecular activation of a Ca2+-dependent protein kinase is disrupted by insertions in the tether that connects the calmodulin-like domain to the kinase. Biochemistry 39, 4004–4011 (2000).

    Article  CAS  PubMed  Google Scholar 

  61. Harper, J. F., Huang, J. F. & Lloyd, S. J. Genetic identification of an autoinhibitor in CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 33, 7267–7277 (1994).

    Article  CAS  PubMed  Google Scholar 

  62. Romeis, T., Ludwig, A. A., Martin, R. & Jones, J. D. G. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20, 5556–5567 (2001). This paper establishes a connection between CDPKs and plant responses to pathogen attack.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Xing, T., Wang, X. J., Malik, K. & Miki, B. L. Ectopic expression of an Arabidopsis calmodulin-like domain protein kinase-enhanced NADPH oxidase activity and oxidative burst in tomato protoplasts. Mol. Plant–Microbe Interact. 14, 1261–1264 (2001).

    Article  CAS  PubMed  Google Scholar 

  64. Morello, L., Frattini, M., Giani, S., Christou, P. & Breviario, D. Overexpression of the calcium-dependent protein kinase OsCDPK2 in transgenic rice is repressed by light in leaves and disrupts seed development. Transgenic Res. 9, 453–462 (2000).

    Article  CAS  PubMed  Google Scholar 

  65. Saijo, Y. et al. A Ca2+-dependent protein kinase that endows rice plants with cold- and salt-stress tolerance functions in vascular bundles. Plant Cell Physiol. 42, 1228–1233 (2001).

    Article  CAS  PubMed  Google Scholar 

  66. Saijo, Y., Hata, S., Kyozuka, J., Shimamoto, K. & Izui, K. Overexpression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J. 23, 319–327 (2000). This paper shows the potential for improving agronomically important stress tolerance traits by changing the expression level of a specific CDPK.

    Article  CAS  PubMed  Google Scholar 

  67. Day, I. S., Reddy, V. S., Shad Ali, G. & Reddy, A. S. Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol. 3, research0056 (2002).

  68. Maser, P. et al. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126, 1646–1667 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Reddy, V. S. & Reddy, A. S. N. Proteomics of calcium-signaling components in plants. Phytochem. 65, 1745–1746 (2004).

    Article  CAS  Google Scholar 

  70. Hwang, I., Sze, H. & Harper, J. F. A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc. Natl Acad. Sci. USA 97, 6224–6229 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Bray, E., Bailey-Serres, J. & Weretilnyk, E. Biochemistry and Molecular Biology of Plants (eds Gruissem, W., Buchannan, B. & Jones, R.) 1158–1203 (American Society of Plant Physiologists, Rockville, Maryland, 2000).

    Google Scholar 

  72. Li, B., Liu, Y., Uno, T. & Gray, N. Creating chemical diversity to target protein kinases. Comb. Chem. High Throughput Screen. 7, 453–472 (2004).

    Article  CAS  PubMed  Google Scholar 

  73. Doerig, C. Protein kinases as targets for anti-parasitic chemotherapy. Biochim. Biophys. Acta 1697, 155–168 (2004).

    Article  CAS  PubMed  Google Scholar 

  74. Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev. Mol. Cell Biol. 4, 517–529 (2003).

    Article  CAS  Google Scholar 

  75. Lacombe, B. et al. The identity of plant glutamate receptors. Science 292, 1486–1487 (2001).

    Article  CAS  PubMed  Google Scholar 

  76. Furuichi, T., Cunningham, K. W. & Muto, S. A putative two pore channel AtTPC1 mediates Ca2+ flux in Arabidopsis leaf cells. Plant Cell Physiol. 42, 900–905 (2001).

    Article  CAS  PubMed  Google Scholar 

  77. Cheng, N. H., Pittman, J. K., Barkla, B. J., Shigaki, T. & Hirschi, K. D. The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15, 347–364 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Wang, D., Harper, J. & Gribskov, M. Trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae. Plant Physiol. 132, 2152–2165 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Plakidou-Dymock, S., Dymock, D. & Hooley, R. A higher plant seven-transmembrane receptor that influences sensitivity to cytokinins. Curr. Biol. 8, 315–324, (1998).

    Article  CAS  PubMed  Google Scholar 

  80. Stoelzle, S., Kagawa, T., Wada, M., Hedrich, R. & Dietrich, P. Blue light activates calcium-permeable channels in Arabidopsis mesophyll cells via the phototropin signaling pathway. Proc. Natl Acad. Sci. USA 100, 1456–1461 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Han, S. C., Tang, R. H., Anderson, L. K., Woerner, T. E. & Pei, Z. M. A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 425, 196–200 (2003).

    Article  CAS  PubMed  Google Scholar 

  82. Ullah, H. et al. Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292, 2066–2069 (2001).

    Article  CAS  PubMed  Google Scholar 

  83. Weiss, C. A., Garnaat, C. W., Mukai, K., Hu, Y. & Ma, H. Isolation of cDNAs encoding guanine nucleotide-binding protein β-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1). Proc. Natl Acad. Sci. USA 91, 9554–9558 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Mason, M. G. & Botella, J. R. Isolation of a novel G-protein γ-subunit from Arabidopsis thaliana and its interaction with Gβ. Biochem. Biophys. Acta 1520, 147–153 (2001).

    CAS  PubMed  Google Scholar 

  85. Mason, M. G. & Botella, J. R. Completing the heterotrimer: Isolation and characterization of an Arabidopsis thaliana G protein γ-subunit cDNA. Proc. Natl Acad. Sci. USA 97, 14784–14788 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Nelson, D. E., Glaunsinger, B. & Bohnert, H. J. Abundant accumulation of the calcium-binding molecular chaperone calreticulin in specific floral tissues of Arabidopsis thaliana. Plant Physiol. 114, 29–37 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Chen, F., Hayes, P. M., Mulrooney, D. M. & Pan, A. Identification and characterization of cDNA clones encoding plant calreticulin in barley. Plant Cell 6, 835–843 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Ehtesham, N. Z., Phan, T. N., Gaikwad, A., Sopory, S. K. & Tuteja, N. Calnexin from Pisum sativum: cloning of the cDNA and characterization of the encoded protein. DNA Cell Biol. 18, 853–862 (1999).

    Article  CAS  PubMed  Google Scholar 

  89. McCormack, E. & Braam, J. Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol. 159, 585–598 (2003).

    Article  CAS  PubMed  Google Scholar 

  90. Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S. & Gruissem, W. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14, S389–S400 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Clark, G. B., Sessions, A., Eastburn, D. J. & Roux, S. J. Differential expression of members of the annexin multigene family in Arabidopsis. Plant Physiol. 126, 1072–1084 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Snedden, W. A. & Fromm, H. Calmodulin as a versatile calcium signal transducer in plants. New Phytol. 151, 35–66 (2001).

    Article  CAS  PubMed  Google Scholar 

  93. Yang, T. & Poovaiah, B. W. Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci. 8, 505–512 (2003).

    Article  CAS  PubMed  Google Scholar 

  94. Zhang, X. R. S. & Choi, J. H. Molecular evolution of calmodulin-like domain protein kinases (CDPKs) in plants and protists. J. Mol. Evolution 53, 214–224 (2001).

    Article  CAS  Google Scholar 

  95. Palmer, J. D., Soltis, D. E. & Chase, D. E. The plant tree of life: an overview and some points of view. Am. J. Botany 91, 1437–1445 (2004).

    Article  Google Scholar 

  96. Hardin, S. C. et al. Phosphorylation of sucrose synthase at serine 170: occurrence and possible role as a signal for proteolysis. Plant J. 35, 588–603 (2003).

    Article  CAS  PubMed  Google Scholar 

  97. Tang, G. Q., Hardin, S. C., Dewey, R. & Huber, S. C. A novel C-terminal proteolytic processing of cytosolic pyruvate kinase, its phosphorylation and degradation by the proteasome in developing soybean seeds. Plant J. 34, 77–93 (2003).

    Article  CAS  PubMed  Google Scholar 

  98. Guenther, J. F. et al. Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15, 981–991 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Lee, S. S. et al. Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J. 33, 825–840 (2003).

    Article  CAS  PubMed  Google Scholar 

  100. Wirth D. F. Biological Revelations. Nature 419, 495–496 (2002).

    Article  CAS  PubMed  Google Scholar 

  101. Roberts, D. M. & Harmon, A. C. Calcium-modulated proteins — targets of intracellular calcium signals in higher plants. Annu. Rev. Plant Physiol. Mol. Biol. 43, 375–414 (1992).

    Article  CAS  Google Scholar 

  102. Neumann, G. M., Thomas, I. & Polya, G. M. Identification of the site on potato carboxypeptidase inhibitor that is phosphorylated by plant calcium-dependent protein kinase. Plant Science 114, 45–51 (1996).

    Article  CAS  Google Scholar 

  103. Huang, J. Z. & Huber, S. C. Phosphorylation of synthetic peptides by a CDPK and plant SNF1-related protein kinase. Influence of proline and basic amino acid residues at selected positions. Plant Cell Physiol. 42, 1079–1087 (2001).

    Article  CAS  PubMed  Google Scholar 

  104. Huang, J. Z., Hardin, S. C. & Huber, S. C. Identification of a novel phosphorylation motif for CDPKs: phosphorylation of synthetic peptides lacking basic residues at P-3/P-4. Arch. Biochem. Biophys. 393, 61–66 (2001).

    Article  CAS  PubMed  Google Scholar 

  105. Loog, M. et al. Peptide phosphorylation by calcium-dependent protein kinase from maize seedlings. Eur. J. Biochem. 267, 337–343 (2000).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are supported by a grant from the National Science Foundation.

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Authors and Affiliations

  1. Department of Biochemistry, MS200, University of Nevada, Reno, 89557, Nevada, USA

    Jeffrey F. Harper

  2. Department of Botany, PO BOX 118526, University of Florida, Gainesville, 32611-8526, Florida, USA

    Alice Harmon

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  1. Jeffrey F. Harper
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Supplementary information

41580_2005_BFnrm1679_MOESM1_ESM.mpg

S1 (movie) | A movie showing Ca2+ oscillations induced by NOD factor in Medicago sativa. The movie shows the injection of an alfalfa (M. sativa) root hair cell with fura-2 dextran dye for detection of Ca2+ concentration changes through fluorescence ratio imaging. The root hair is then exposed to a Nod factor that triggers a periodic Ca2+ release in the vicinity of the nucleus. Mutations that block this Ca2+ signal have also been found to block the ability of the root hair to initiate bacterial and fungal symbiotic relationships. This movie is provided with the permission of D. W. Ehrhardt and S. R. Long, Department of Biological Sciences, Stanford University, USA. (MPG 1715 kb)

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DATABASES

Prosite

EF-hands

FURTHER INFORMATION

PlantsP

Glossary

POLLEN TUBE

A tube that grows from the pollen grain through the style to the ovule. The tube transports the male gametes into the ovule to fertilize the egg cell.

CALMODULIN

A Ca2+-binding protein that contains four Ca2+-binding EF-hands. Calmodulin binds various protein targets in the presence of micromolar Ca2+, modulates the activity or function of the targets and affects many cellular functions.

PROTISTS

Mostly unicellular organisms that include protozoa and algae, and that diverged in evolution before plants, animals and fungi.

REVERSE GENETICS

An approach for discovering the function of genes in which a mutation in a particular gene is identified first, and the phenotype resulting from the mutation is characterized afterwards.

FORWARD GENETICS

An approach for discovering the function of genes in which mutant phenotypes are identified first, and the mutant gene responsible for the phenotype is identified later.

EF-HAND

A structure in proteins that binds Ca2+ with high affinity and selectivity.

VISININ

A protein that contains Ca2+-binding EFhands and which is a member of the neuronal Ca2+-sensor protein family.

APICOMPLEXA

A group of protists that together with ciliates and dinoflagellates comprise alveolates, a group of organisms that have small membrane-bound cavities under their cell surfaces.

MONOCOTS

Flowering plants that have one seed leaf and that diverged in evolution from basal angiosperms.

EUDICOTS

('True dicots'). A large subgroup of flowering plants that have two cotyledons (seed leaves) and that diverged in evolution after the appearance of monocots. Recent DNA evidence shows that the plant group formerly called dicots can be divided into eudicots and basal angiosperms, which appeared before monocots.

CILIATES

A type of protist that moves by means of cellular projections called cilia.

MYRISTOYLATION

A type of protein modification in which myristic acid, a 14-carbon fatty acid, is covalenty attached to the protein.

PALMITOYLATION

A type of protein modification in which palmitic acid, a 16-carbon fatty acid, is covalently attached to the protein.

PEROXISOMES

Organelles that produce and use hydrogen peroxide.

OIL BODIES

Storage organelles containing triacylglycerides, which are derived from the endoplasmic reticulum and found in the fleshy parts (endosperm or cotyledons) of seeds.

14-3-3 PROTEINS

A family of conserved proteins that are involved in diverse cellular processes including intracellular signalling and cell-cycle regulation. 143-3 proteins function as adaptors in protein interactions and can regulate protein localization and enzymatic activity.

26S PROTEOSOME

A eukaryotic assembly of proteins that degrades other proteins.

CYTOPLASMIC STREAMING

The movement of cytoplasm in a plant or animal cell that transports intracellular components such as nutrients and enzymes in the cell.

POLLEN MOTHER CELL

A cell (also called a microsporocyte) that is located in the anther. These cells divide by meiosis to give rise to the four haploid microspores, the precursors of the pollen grain.

PROTOPLASTS

Plant cells with the cell wall artificially removed.

HYPERSENSITIVE RESPONSE

A complex, early defence response that causes cell death to restrict the growth of a pathogen.

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Harper, J., Harmon, A. Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6, 555–566 (2005). https://doi.org/10.1038/nrm1679

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