Calcium Signaling and Homeostasis in Nuclei

  • Christian MazarsEmail author
  • Patrice Thuleau
  • Valérie Cotelle
  • Christian Brière
Part of the Signaling and Communication in Plants book series (SIGCOMM)


Calcium variations occurring in the nucleus and in other calcium-active compartments of the plant cell are contributing to encode information of specificity used by the cell to mount an appropriate response to environmental cues. This chapter deals with calcium signaling in the nucleus and reports on the current knowledge on calcium signals monitored in plant cell nuclei in response to biotic and abiotic stimuli. On the basis of both the experimental and modeling data, evidences of the autonomy of the nucleus which is able to generate its own calcium signals and to maintain its calcium homeostasis by itself are brought. Finally, the biological relevance of such nuclear calcium signals is discussed with regard to the nuclear sub-compartments and the biological activities which are taking place in these sub-compartments.


Calcium Signal Perinuclear Space Nuclear Calcium Electron Multiply Couple Charge Device Plant Cell Nucleus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057PubMedCrossRefGoogle Scholar
  2. al-Mohanna FA, Caddy KW, Bolsover SR (1994) The nucleus is insulated from large cytosolic calcium ion changes. Nature 367:745–750PubMedCrossRefGoogle Scholar
  3. Badminton MN, Kendall JM, Sala-Newby G, Campbell AK (1995) Nucleoplasmin-targeted aequorin provides evidence for a nuclear calcium barrier. Exp Cell Res 216:236–243PubMedCrossRefGoogle Scholar
  4. Badminton MN, Campbell AK, Rembold CM (1996) Differential regulation of nuclear and cytosolic Ca2+ in HeLa cells. J Biol Chem 271:31210–31214PubMedCrossRefGoogle Scholar
  5. Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924PubMedCrossRefGoogle Scholar
  6. Batistic O, Kudla J (2009) Plant calcineurin B-like proteins and their interacting protein kinases. Biochim Biophys Acta 1793:985–992PubMedCrossRefGoogle Scholar
  7. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21PubMedCrossRefGoogle Scholar
  8. Bootman MD, Thomas D, Tovey SC, Berridge MJ, Lipp P (2000) Nuclear calcium signalling. Cell Mol Life Sci 57:371–378PubMedCrossRefGoogle Scholar
  9. Bouché N, Scharlat A, Snedden W, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851–21861PubMedCrossRefGoogle Scholar
  10. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–422PubMedCentralPubMedCrossRefGoogle Scholar
  11. Brière C, Xiong TC, Mazars C, Ranjeva R (2004) Autonomous regulation of free Ca2+ concentrations in isolated plant cell nuclei: a mathematical analysis. Cell Calcium 39:293–303.CrossRefGoogle Scholar
  12. Brini M, Murgia M, Pasti L, Picard D, Pozzan T, Rizzuto R (1993) Nuclear Ca2+ concentration measured with specifically targeted recombinant aequorin. EMBO J 12:4813–4819PubMedGoogle Scholar
  13. Cardenas C, Liberona JL, Molgo J, Colasante C, Mignery GA, Jaimovich E (2005) Nuclear inositol 1,4,5-trisphosphate receptors regulate local Ca2+ transients and modulate cAMP response element binding protein phosphorylation. J Cell Sci 118:3131–3140PubMedCrossRefGoogle Scholar
  14. Charon C, Moreno AB, Bardou F, Crespi M (2010) Non-protein-coding RNAs and their interacting RNA-binding proteins in the plant cell nucleus. Mol Plant 3:729–739Google Scholar
  15. Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20:3467–3479PubMedCentralPubMedCrossRefGoogle Scholar
  16. Cho W, Stahelin RV (2006) Membrane binding and subcellular targeting of C2 domains. Biochim Biophys Acta 1761:838–849PubMedCrossRefGoogle Scholar
  17. Clapham DE, Runnels LW, Strubing C (2001) The TRP ion channel family. Nat Rev Neurosci 2:387–396PubMedCrossRefGoogle Scholar
  18. Collings DA, Carter CN, Rink JC, Scott AC, Wyatt SE, Allen NS (2000) Plant nuclei can contain extensive grooves and invaginations. Plant Cell 12:2425–2440PubMedCentralPubMedGoogle Scholar
  19. Dahan J, Wendehenne D, Ranjeva R, Pugin A, Bourque S (2010) Nuclear protein kinases: still enigmatic components in plant cell signalling. New Phytol 185:355–368PubMedCrossRefGoogle Scholar
  20. Dammann C, Ichida A, Hong B, Romanowsky SM, Hrabak EM, Harmon AC, Pickard BG, Harper JF (2003) Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol 132:1840–1848PubMedCentralPubMedCrossRefGoogle Scholar
  21. Day IS, Reddy VS, Shad Ali G, Reddy AS (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol 3:56CrossRefGoogle Scholar
  22. Downie L, Priddle J, Hawes C, Evans DE (1998) A calcium pump at the higher plant nuclear envelope? FEBS Lett 429:44–48PubMedCrossRefGoogle Scholar
  23. Echevarria W, Leite MF, Guerra MT, Zipfel WR, Nathanson MH (2003) Regulation of calcium signals in the nucleus by a nucleoplasmic reticulum. Nat Cell Biol 5:440–446PubMedCentralPubMedCrossRefGoogle Scholar
  24. Finkler A, Ashery-Padan R, Fromm H (2007) CAMTAs: Calmodulin-binding transcription activators from plants to human. FEBS Lett 581:3893–3898PubMedCrossRefGoogle Scholar
  25. Fiserova J, Kiseleva E, Goldberg MW (2009) Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells. Plant J 59:243–255PubMedCrossRefGoogle Scholar
  26. Galon Y, Finkler A, Fromm H (2009) Calcium-regulated transcription in plants. Mol Plant 3:653–669Google Scholar
  27. Gleason C, Chaudhuri S, Yang T, Munoz A, Poovaiah BW, Oldroyd GE (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441:1149–1152PubMedCrossRefGoogle Scholar
  28. Goldberg MW, Allen TD (1996) The nuclear pore complex and lamina: three-dimensional structures and interactions determined by field emission in-lens scanning electron microscopy. J Mol Biol 257:848–865PubMedCrossRefGoogle Scholar
  29. Grygorczyk C, Grygorczyk R (1998) A Ca2+- and voltage-dependent cation channel in the nuclear envelope of red beet. Biochim Biophys Acta Biomembr 1375:117–130CrossRefGoogle Scholar
  30. Hager GL, McNally JG, Misteli T (2009) Transcription dynamics. Mol Cell 35:741–753PubMedCrossRefGoogle Scholar
  31. Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288PubMedCrossRefGoogle Scholar
  32. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680PubMedCentralPubMedCrossRefGoogle Scholar
  33. Hsieh HL, Song CJ, Roux SJ (2000) Regulation of a recombinant pea nuclear apyrase by calmodulin and casein kinase II. Biochim Biophys Acta 1494:248–255PubMedCrossRefGoogle Scholar
  34. Inaba T (2010) Bilateral communication between plastid and the nucleus: plastid protein import and plastid-to-nucleus retrograde signaling. Biosci Biotechnol Biochem 74:471–476PubMedCrossRefGoogle Scholar
  35. Inouye S, Noguchi M, Sakaki Y, Takagi Y, Miyata T, Iwanaga S, Miyata T, Tsuji FI (1985) Cloning and sequence analysis of cDNA for the luminescent protein aequorin. Proc Natl Acad Sci USA 82:3154–3158PubMedCrossRefGoogle Scholar
  36. Johnson C, Knight M, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269:1863–1865PubMedCrossRefGoogle Scholar
  37. Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell 18:2733–2748PubMedCentralPubMedCrossRefGoogle Scholar
  38. Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21PubMedCrossRefGoogle Scholar
  39. Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526PubMedCrossRefGoogle Scholar
  40. Krishtal O (2003) The ASICs: signaling molecules? Modulators? Trends Neurosci 26:477–483PubMedCrossRefGoogle Scholar
  41. Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563PubMedCentralPubMedCrossRefGoogle Scholar
  42. Lachaud C, Da Silva D, Cotelle V, Thuleau P, Xiong TC, Jauneau A, Briere C, Graziana A, Bellec Y, Faure JD, Ranjeva R, Mazars C (2010) Nuclear calcium controls the apoptotic-like cell death induced by d-erythro-sphinganine in tobacco cells. Cell Calcium 47:92–100PubMedCrossRefGoogle Scholar
  43. Lange A, Mills RE, Lange CJ, Stewart M, Devine SE, Corbett AH (2007) Classical nuclear localization signals: definition, function, and interaction with importin alpha. J Biol Chem 282:5101–5105PubMedCrossRefGoogle Scholar
  44. Laude AJ, Simpson AW (2009) Compartmentalized signalling: Ca2+ compartments, microdomains and the many facets of Ca2+ signalling. FEBS J 276:1800–1816PubMedCrossRefGoogle Scholar
  45. Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14:2627–2641PubMedCentralPubMedCrossRefGoogle Scholar
  46. Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, Ranjeva R, Pugin A (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38:527–538PubMedCrossRefGoogle Scholar
  47. Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269PubMedCrossRefGoogle Scholar
  48. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784PubMedCrossRefGoogle Scholar
  49. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet E-P, Ane J-M, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364PubMedCrossRefGoogle Scholar
  50. Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21–24PubMedCentralPubMedCrossRefGoogle Scholar
  51. Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14:37–42PubMedCrossRefGoogle Scholar
  52. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14(Suppl):S389–S400PubMedCentralPubMedGoogle Scholar
  53. Malviya AN (1994) The nuclear inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate receptors. Cell Calcium 16:301–313PubMedCrossRefGoogle Scholar
  54. Matzke M, Aufsatz W, Gregor W, van Der Winden J, Papp I, Matzke AJ (2001) Ion transporters in the nucleus? Plant Physiol 127:10–13PubMedCentralPubMedCrossRefGoogle Scholar
  55. Matzke M, Weiger TM, Papp I, Matzke AJ (2009) Nuclear membrane ion channels mediate root nodule development. Trends Plant Sci 14:295–298PubMedCrossRefGoogle Scholar
  56. McAinsh MR, Hetherington AM (1998) Encoding specificity in Ca2+ signalling systems. Trends Plant Sci 3:32–36CrossRefGoogle Scholar
  57. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294PubMedCrossRefGoogle Scholar
  58. Mehlmer N, Wurzinger B, Stael S, Hofmann-Rodrigues D, Csaszar E, Pfister B, Bayer R, Teige M (2010) The Ca2+-dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. Plant J 63:484–498Google Scholar
  59. Meier I (2007) Composition of the plant nuclear envelope: theme and variations. J Exp Bot 58:27–34PubMedCrossRefGoogle Scholar
  60. Meier I, Brkljacic J (2009) The nuclear pore and plant development. Curr Opin Plant Biol 12:87–95PubMedCrossRefGoogle Scholar
  61. Messinese E, Mun JH, Yeun LH, Jayaraman D, Rouge P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ane JM (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20:912–921PubMedCrossRefGoogle Scholar
  62. Misteli T (2001) Protein dynamics: implications for nuclear architecture and gene expression. Science 291:843–847PubMedCrossRefGoogle Scholar
  63. Mithofer A, Mazars C (2002) Aequorin-based measurements of intracellular Ca2+-signatures in plant cells. Biol Proced Online 4:105–118PubMedCentralPubMedCrossRefGoogle Scholar
  64. Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705PubMedCrossRefGoogle Scholar
  65. Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48:883–894PubMedCrossRefGoogle Scholar
  66. Nakajima-Shimada J, Iida H, Tsuji FI, Anraku Y (1991) Monitoring of intracellular calcium in Saccharomyces cerevisiae with an apoaequorin cDNA expression system. Proc Natl Acad Sci USA 88:6878–6882PubMedCrossRefGoogle Scholar
  67. Nakayama S, Kretsinger RH (1994) Evolution of the EF-hand family of proteins. Annu Rev Biophys Biomol Struct 23:473–507PubMedCrossRefGoogle Scholar
  68. Ng CK, McAinsh MR (2003) Encoding specificity in plant calcium signalling: hot-spotting the ups and downs and waves. Ann Bot 92:477–485PubMedCrossRefGoogle Scholar
  69. O’Malley DM, Burbach BJ, Adams PR (1999) Fluorescent calcium indicators: subcellular behavior and use in confocal imaging. Methods Mol Biol 122:261–303PubMedGoogle Scholar
  70. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546PubMedCrossRefGoogle Scholar
  71. Pauly N, Knight MR, Thuleau P, van der Luit AH, Moreau M, Trewavas AJ, Ranjeva R, Mazars C (2000) Cell signalling: control of free calcium in plant cell nuclei. Nature 405:754–755PubMedCrossRefGoogle Scholar
  72. Pauly N, Knight MR, Thuleau P, Graziana A, Muto S, Ranjeva R, Mazars C (2001) The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 30:413–421PubMedCrossRefGoogle Scholar
  73. Perez-Terzic C, Jaconi M, Clapham DE (1997) Nuclear calcium and the regulation of the nuclear pore complex. Bioessays 19:787–792PubMedCrossRefGoogle Scholar
  74. Perruc E, Charpenteau M, Ramirez BC, Jauneau A, Galaud J-P, Ranjeva R, Ranty B (2004) A novel calmodulin-binding protein functions as a negative regulator of osmotic stress tolerance in Arabidopsis thaliana seedlings. Plant J 38:410–420PubMedCrossRefGoogle Scholar
  75. Phair RD, Gorski SA, Misteli T (2004) Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol 375:393–414PubMedCrossRefGoogle Scholar
  76. Reddy AS, Day IS, Narasimhulu SB, Safadi F, Reddy VS, Golovkin M, Harnly MJ (2002) Isolation and characterization of a novel calmodulin-binding protein from potato. J Biol Chem 277:4206–4214PubMedCrossRefGoogle Scholar
  77. Rizzuto R, Brini M, Pozzan T (1993) Intracellular targeting of the photoprotein aequorin: a new approach for measuring, in living cells, Ca2+ concentrations in defined cellular compartments. Cytotechnology 11(Suppl 1):S44–S46CrossRefGoogle Scholar
  78. Rodrigues MA, Gomes DA, Nathanson MH, Leite MF (2009) Nuclear calcium signaling: a cell within a cell. Braz J Med Biol Res 42:17–20PubMedCentralPubMedCrossRefGoogle Scholar
  79. Rodriguez-Concepcion M, Yalovsky S, Zik M, Fromm H, Gruissem W (1999) The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein. EMBO J 18:1996–2007PubMedCrossRefGoogle Scholar
  80. Saez-Vasquez J, Gadal O (2010) Genome organization and function: a view from yeast and Arabidopsis. Mol Plant 3:678–690Google Scholar
  81. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401–S417PubMedCentralPubMedGoogle Scholar
  82. Sathyanarayanan PV, Cremo CR, Poovaiah BW (2000) Plant chimeric Ca2+/Calmodulin-dependent Protein Kinase. J Biol Chem 275:30417–30422PubMedCrossRefGoogle Scholar
  83. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658PubMedCrossRefGoogle Scholar
  84. Scrase-Field SA, Knight MR (2003) Calcium: just a chemical switch? Curr Opin Plant Biol 6:500–506PubMedCrossRefGoogle Scholar
  85. Shaw PJ, Brown JW (2004) Plant nuclear bodies. Curr Opin Plant Biol 7:614–620PubMedCrossRefGoogle Scholar
  86. Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59:223–239PubMedCrossRefGoogle Scholar
  87. Sieberer BJ, Chabaud M, Timmers AC, Monin A, Fournier J, Barker DG (2009) A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151:1197–1206PubMedCentralPubMedCrossRefGoogle Scholar
  88. Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791PubMedCrossRefGoogle Scholar
  89. Spector DL (2001) Nuclear domains. J Cell Sci 114:2891–2893PubMedGoogle Scholar
  90. Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71PubMedCrossRefGoogle Scholar
  91. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665PubMedCrossRefGoogle Scholar
  92. Thomas D, Tovey SC, Collins TJ, Bootman MD, Berridge MJ, Lipp P (2000) A comparison of fluorescent Ca2+ indicator properties and their use in measuring elementary and global Ca2+ signals. Cell Calcium 28:213–223PubMedCrossRefGoogle Scholar
  93. van der Luit AH, Olivari C, Haley A, Knight MR, Trewavas AJ (1999) Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiol 121:705–714PubMedCentralCrossRefGoogle Scholar
  94. Walker SA, Viprey V, Downie JA (2000) Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proc Natl Acad Sci USA 97:13413–13418PubMedCrossRefGoogle Scholar
  95. Walter A, Mazars C, Maitrejean M, Hopke J, Ranjeva R, Boland W, Mithöfer A (2007) Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. Angew Chem Int Ed 46:4783–4785CrossRefGoogle Scholar
  96. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697PubMedCrossRefGoogle Scholar
  97. Weinl S, Kudla J (2009) The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528PubMedCrossRefGoogle Scholar
  98. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511PubMedCrossRefGoogle Scholar
  99. Xiong TC, Jauneau A, Ranjeva R, Mazars C (2004) Isolated plant nuclei as mechanical and thermal sensors involved in calcium signalling. Plant J 40:12–21PubMedCrossRefGoogle Scholar
  100. Xiong T-C, Bourque S, Lecourieux D, Amelot N, Grat S, Brière C, Mazars C, Pugin A, Ranjeva R (2006) Calcium signaling in plant cell organelles delimited by a double membrane. Biochim Biophys Acta 1763:1209–1215PubMedCrossRefGoogle Scholar
  101. Xiong TC, Coursol S, Grat S, Ranjeva R, Mazars C (2008) Sphingolipid metabolites selectively elicit increases in nuclear calcium concentration in cell suspension cultures and in isolated nuclei of tobacco. Cell Calcium 43:29–37PubMedCrossRefGoogle Scholar
  102. Xu XM, Meier I (2008) The nuclear pore comes to the fore. Trends Plant Sci 13:20–27PubMedCrossRefGoogle Scholar
  103. Yoo SH, Nam SW, Huh SK, Park SY, Huh YH (2005) Presence of a nucleoplasmic complex composed of the inositol 1,4,5-trisphosphate receptor/Ca2+ channel, chromogranin B, and phospholipids. Biochemistry 44:9246–9254PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Christian Mazars
    • 1
    • 2
    Email author
  • Patrice Thuleau
    • 1
    • 2
  • Valérie Cotelle
    • 1
    • 2
  • Christian Brière
    • 1
    • 2
  1. 1.Laboratoire de Recherche en Sciences VégétalesUniversité de Toulouse, UPS, UMR 5546Castanet-TolosanFrance
  2. 2.CNRS, UMR 5546Castanet-TolosanFrance

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