Skip to main content
Log in

The role of calcium in chloroplasts—an intriguing and unresolved puzzle

  • Review Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

More than 70 years of studies have indicated that chloroplasts contain a significant amount of calcium, are a potential storage compartment for this ion, and might themselves be prone to calcium regulation. Many of these studies have been performed on the photosynthetic light reaction as well as CO2 fixation via the Calvin–Benson–Bassham cycle, and they showed that calcium is required in several steps of these processes. Further studies have indicated that calcium is involved in other chloroplast functions that are not directly related to photosynthesis and that there is a calcium-dependent regulation similar to cytoplasmic calcium signal transduction. Nevertheless, the precise role that calcium has as a functional and regulatory component of chloroplast processes remains enigmatic. Calcium concentrations in different chloroplast subcompartments have been measured, but the extent and direction of intra-plastidal calcium fluxes or calcium transport into and from the cytosol are not yet very well understood. In this review we want to give an overview over the current knowledge on the relationship between chloroplasts and calcium and discuss questions that need to be addressed in future research.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

CaM:

Calmodulin

CBB:

Calvin–Benson–Bassham cycle

CAS:

Calcium-sensing protein

CRSH:

(p)ppGpp synthases–degradases

FBPase:

Fructose-1,6-bisphosphatase

FDX:

Ferredoxin

GECI:

Genetically encoded calcium indicator

NADK:

NAD kinase

(p)ppGpp:

Guanosine 5′-triphosphate (or 5′-diphosphate) 3′-diphosphate

PSI/II:

Photosystem I/II

PSA/PSB:

Component of PSI/II

SBPase:

Sedoheptulose-l,7-biphosphatase

TIC:

Translocon on the inner envelope of chloroplast

References

  • Anderson JM, Charbonneau H, Jones HP, McCann RO, Cormier MJ (1980) Characterization of the plant nicotinamide adenine dinucleotide kinase activator protein and its identification as calmodulin. Biochemistry 19(13):3113–3120

    Article  PubMed  CAS  Google Scholar 

  • Aro E-M, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56(411):347–356. doi:10.1093/jxb/eri041

    Article  PubMed  CAS  Google Scholar 

  • Balsera M, Goetze TA, Kovacs-Bogdan E, Schurmann P, Wagner R, Buchanan BB, Soll J, Bolter B (2009) Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca(2+) and a stromal regulatory disulfide bridge. J Biol Chem 284(5):2603–2616. doi:10.1074/jbc.M807134200

    Article  PubMed  CAS  Google Scholar 

  • Bayer RG, Stael S, Csaszar E, Teige M (2011a) Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11(7):1287–1299. doi:10.1002/pmic.201000495

    Article  PubMed  CAS  Google Scholar 

  • Bayer RG, Stael S, Rocha A, Mair A, Vothknecht UC, Teige M (2011b) Chloroplast localised protein kinases—a step forward towards a complete inventory. J Exp Bot. doi:10.1093/jxb/err377

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1(1):11–21. doi:10.1038/35036035

    Article  PubMed  CAS  Google Scholar 

  • Bertsch U, Soll J (1995) Functional analysis of isolated cpn10 domains and conserved amino acid residues in spinach chloroplast co-chaperonin by site-directed mutagenesis. Plant Mol Biol 29(5):1039–1055

    Article  PubMed  CAS  Google Scholar 

  • Brand JJ, Becker DW (1984) Evidence for direct roles of calcium in photosynthesis. J Bioenerg Biomembr 16(4):239–249

    Article  PubMed  CAS  Google Scholar 

  • Buaboocha T, Liao B, Zielinski RE (2001) Isolation of cDNA and genomic DNA clones encoding a calmodulin-binding protein related to a family of ATPases involved in cell division and vesicle fusion. Planta 212(5–6):774–781

    Article  PubMed  CAS  Google Scholar 

  • Bussemer J, Chigri F, Vothknecht UC (2009a) Arabidopsis ATPase family gene 1-like protein 1 is a calmodulin-binding AAA+-ATPase with a dual localization in chloroplasts and mitochondria. FEBS J 276(14):3870–3880. doi:10.1111/j.1742-4658.2009.07102.x

    Article  PubMed  CAS  Google Scholar 

  • Bussemer J, Vothknecht UC, Chigri F (2009b) Calcium regulation in endosymbiotic organelles of plants. Plant Signal Behav 4(9):805–808

    Article  PubMed  CAS  Google Scholar 

  • Cadet F, Meunier JC (1988) Spinach (Spinacia oleracea) chloroplast sedoheptulose-1,7-bisphosphatase. Activation and deactivation, and immunological relationship to fructose-1,6-bisphosphatase. Biochem J 253(1):243–248

    PubMed  CAS  Google Scholar 

  • Chardot T, Meunier JC (1990) Fructose-1,6-bisphosphate and calcium activate oxidized spinach (Spinacia oleracea) chloroplast fructose-1,6-bisphosphatase. Plant Sci 70(1):1–9

    Article  CAS  Google Scholar 

  • Charles SA, Halliwell B (1980) Action of calcium ions on spinach (Spinacia oleracea) chloroplast fructose bisphosphatase and other enzymes of the Calvin cycle. Biochem J 188(3):775–779

    PubMed  CAS  Google Scholar 

  • Chen C, Kazimir J, Cheniae GM (1995) Calcium modulates the photoassembly of photosystem II (Mn)4-clusters by preventing ligation of nonfunctional high-valency states of manganese. Biochemistry 34(41):13511–13526

    Article  PubMed  CAS  Google Scholar 

  • Chigri F, Soll J, Vothknecht UC (2005) Calcium regulation of chloroplast protein import. Plant J 42(6):821–831. doi:10.1111/j.1365-313X.2005.02414.x

    Article  PubMed  CAS  Google Scholar 

  • Chigri F, Hormann F, Stamp A, Stammers DK, Bolter B, Soll J, Vothknecht UC (2006) Calcium regulation of chloroplast protein translocation is mediated by calmodulin binding to Tic32. Proc Natl Acad Sci U S A 103(43):16051–16056. doi:10.1073/pnas.0607150103

    Article  PubMed  CAS  Google Scholar 

  • Chigri F, Flosdorff S, Pilz S, Kolle E, Dolze E, Gietl C, Vothknecht UC (2011) The Arabidopsis calmodulin-like proteins AtCML30 and AtCML3 are targeted to mitochondria and peroxisomes, respectively. Plant Mol Biol. doi:10.1007/s11103-011-9856-z

  • Chitnis PR (2001) Photosystem I: function and physiology. Annu Rev Plant Physiol Plant Mol Biol 52:593–626

    Article  PubMed  CAS  Google Scholar 

  • Clapham DE (2007) Calcium signaling. Cell 131(6):1047–1058. doi:10.1016/j.cell.2007.11.028

    Article  PubMed  CAS  Google Scholar 

  • DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425:27–40. doi:10.1042/Bj20091147

    Article  CAS  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620. doi:10.1146/annurev-arplant-070109-104628

    Article  PubMed  CAS  Google Scholar 

  • Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392(6679):933–936. doi:10.1038/31960

    Article  PubMed  CAS  Google Scholar 

  • Dunkley TPJ, Hester S, Shadforth IP, Runions J, Weimar T, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, Watson RB, Dupree P, Lilley KS (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci 103(17):6518–6523. doi:10.1073/pnas.0506958103

    Article  PubMed  CAS  Google Scholar 

  • Enz C, Steinkamp T, Wagner R (1993) Ion channels in the thylakoid membrane (a patch-clamp study). Biochim Biophys Acta 1143(1):67–76

    Article  CAS  Google Scholar 

  • Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119(4):1379–1386

    Article  PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303(5665):1831–1838. doi:10.1126/science.1093087

    Article  PubMed  CAS  Google Scholar 

  • Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2(5):325–345. doi:10.1074/mcp.M300005-MCP200

    PubMed  CAS  Google Scholar 

  • Ghanotakisa DF, Babcockb GT, Yocuma CF (1984) Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations. FEBS Lett 167(1):127–130. doi:10.1016/0014-5793(84)80846-7

    Article  Google Scholar 

  • Han S, Tang R, Anderson LK, Woerner TE, Pei Z-M (2003) A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 425(6954):196–200, http://www.nature.com/nature/journal/v425/n6954/suppinfo/nature01932_S1.html

    Article  PubMed  CAS  Google Scholar 

  • Heredia P, De Las Rivas J (2003) Calcium-dependent conformational change and thermal stability of the isolated PsbO protein detected by FTIR spectroscopy. Biochemistry 42(40):11831–11838. doi:10.1021/bi034582j

    Article  PubMed  CAS  Google Scholar 

  • Hertig C, Wolosiuk RA (1980) A dual effect of Ca2+ on chloroplast fructose-1,6-bisphosphatase. Biochem Biophys Res Commun 97(1):325–333

    Article  PubMed  CAS  Google Scholar 

  • Hertig CM, Wolosiuk RA (1983) Studies on the hysteretic properties of chloroplast fructose-1,6-bisphosphatase. J Biol Chem 258(2):984–989

    PubMed  CAS  Google Scholar 

  • Huang L, Berkelman T, Franklin AE, Hoffman NE (1993) Characterization of a gene encoding a Ca(2+)-ATPase-like protein in the plastid envelope. Proc Natl Acad Sci U S A 90(21):10066–10070

    Article  PubMed  CAS  Google Scholar 

  • Ifuku K, Yamamoto Y, Ono TA, Ishihara S, Sato F (2005) PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. Plant Physiol 139(3):1175–1184. doi:10.1104/pp.105.068643

    Article  PubMed  CAS  Google Scholar 

  • Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269(5232):1863–1865

    Article  PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krausz N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5[thinsp][angst] resolution. Nature 411(6840):909–917, http://www.nature.com/nature/journal/v411/n6840/suppinfo/411909a0_S1.html

    Article  PubMed  CAS  Google Scholar 

  • Kasai K, Usami S, Yamada T, Endo Y, Ochi K, Tozawa Y (2002) A RelA-SpoT homolog (Cr-RSH) identified in Chlamydomonas reinhardtii generates stringent factor in vivo and localizes to chloroplasts in vitro. Nucleic Acids Res 30(22):4985–4992

    Article  PubMed  CAS  Google Scholar 

  • Kasai K, Kanno T, Endo Y, Wakasa K, Tozawa Y (2004) Guanosine tetra- and pentaphosphate synthase activity in chloroplasts of a higher plant: association with 70S ribosomes and inhibition by tetracycline. Nucleic Acids Res 32(19):5732–5741. doi:10.1093/nar/gkh916

    Article  PubMed  CAS  Google Scholar 

  • 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(6335):524–526. doi:10.1038/352524a0

    Article  PubMed  CAS  Google Scholar 

  • Kovács-Bogdán E, Soll J, Bölter B (2010) Protein import into chloroplasts: the Tic complex and its regulation. Biochim Biophys Acta 1803(6):740–747. doi:10.1016/j.bbamcr.2010.01.015

    Article  PubMed  Google Scholar 

  • Kreimer G, Melkonian M, Latzko E (1985) An electrogenic uniport mediates light-dependent Ca2+ influx into intact spinach chloroplasts. FEBS Lett 180(2):253–258. doi:10.1016/0014-5793(85)81081-4

    Article  CAS  Google Scholar 

  • Kreimer G, Melkonian M, Holtum JA, Latzko E (1988) Stromal free calcium concentration and light-mediated activation of chloroplast fructose-1,6-bisphosphatase. Plant Physiol 86:423–428

    Article  PubMed  CAS  Google Scholar 

  • Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of Photosystem II. Photosynth Res 37(2):117–130. doi:10.1007/bf02187470

    Article  CAS  Google Scholar 

  • Kruk J, Burda K, Jemioła-Rzemińska M, Strzałka K (2003) The 33 kDa protein of photosystem II is a low-affinity calcium- and lanthanide-binding protein. Biochemistry 42(50):14862–14867. doi:10.1021/bi0351413

    Article  PubMed  CAS  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22(3):541–563. doi:10.1105/tpc.109.072686

    Article  PubMed  CAS  Google Scholar 

  • Larkum AWD (1968) Ionic relations of chloroplasts in vivo. Nature 218(5140):447–449

    Article  CAS  Google Scholar 

  • Li W, Llopis J, Whitney M, Zlokarnik G, Tsien RY (1998) Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature 392(6679):936–941. doi:10.1038/31965

    Article  PubMed  CAS  Google Scholar 

  • Masuda S, Tozawa Y, Ohta H (2008) Possible targets of “magic spots” in plant signalling. Plant Signal Behav 3(11):1021–1023

    Google Scholar 

  • McAinsh MR, Webb A, Taylor JE, Hetherington AM (1995) Stimulus-induced oscillations in guard cell cytosolic free calcium. Plant Cell 7(8):1207–1219. doi:10.1105/tpc.7.8.1207

    PubMed  CAS  Google Scholar 

  • McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159(3):585–598. doi:doi:10.1046/j.1469-8137.2003.00845.x

    Article  CAS  Google Scholar 

  • McNamara VP, Gounaris K (1995) Granal photosystem II complexes contain only the high redox potential form of cytochrome b-559 which is stabilised by the ligation of calcium. Biochim Biophys Acta 1231(3):289–296. doi:10.1016/0005-2728(95)00093-x

    Article  Google Scholar 

  • Mehlmer N, Parvin N, Hurst CH, Knight MR, Teige M, Vothknecht UC (2011) A toolset of aequorin expression vectors for in planta studies of subcellular calcium concentrations in Arabidopsis thaliana. J Exp Bot. doi:10.1093/jxb/err406

  • Miqyass M, van Gorkom H, Yocum C (2007) The PSII calcium site revisited. Photosynth Res 92(3):275–287. doi:10.1007/s11120-006-9124-2

    Article  PubMed  CAS  Google Scholar 

  • Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388(6645):882–887

    Article  PubMed  CAS  Google Scholar 

  • Moreno I, Norambuena L, Maturana D, Toro M, Vergara C, Orellana A, Zurita-Silva A, Ordenes VR (2008) AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J Biol Chem 283(15):9633–9641. doi:10.1074/jbc.M800736200

    Article  PubMed  CAS  Google Scholar 

  • Murray JW, Barber J (2006) Identification of a calcium-binding site in the PsbO protein of photosystem II. Biochemistry 45(13):4128–4130. doi:10.1021/bi052503t

    Article  PubMed  CAS  Google Scholar 

  • Muto S, Izawa S, Miyachi S (1982) Light-induced Ca2+ uptake by intact chloroplasts. FEBS Lett 139(2):250–254

    Article  CAS  Google Scholar 

  • Neish AC (1939) Studies on chloroplasts. II. Their chemical composition and the distribution of certain metabolites between the chloroplasts and the remainder of the leaf. Biochem J 33:300–308

    PubMed  CAS  Google Scholar 

  • Nobel PS (1969) Light-induced changes in the ionic content of chloroplasts in Pisum sativum. Biochim Biophys Acta 172(1):134–143. doi:10.1016/0005-2728(69)90098-x

    Article  PubMed  CAS  Google Scholar 

  • Nobel PS, Murakami S, Takamiya A (1966) Localization of light-induced strontium accumulation in spinach chloroplasts. Plant Cell Physiol 7(2):263–275

    CAS  Google Scholar 

  • Nomura H, Komori T, Kobori M, Nakahira Y, Shiina T (2008) Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 53(6):988–998. doi:10.1111/j.1365-313X.2007.03390.x

    Article  PubMed  CAS  Google Scholar 

  • O'Keefe DP, Dilley RA (1977) The effect of chloroplast coupling factor removal on thylakoid membrane ion permeability. Biochim Biophys Acta 461(1):48–60. doi:10.1016/0005-2728(77)90068-8

    Article  PubMed  Google Scholar 

  • Peltier J-B, Ytterberg AJ, Sun Q, van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279(47):49367–49383. doi:10.1074/jbc.M406763200

    Article  PubMed  CAS  Google Scholar 

  • Petroutsos D, Busch A, Janssen I, Trompelt K, Bergner SV, Weinl S, Holtkamp M, Karst U, Kudla J, Hippler M (2011) The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. Plant Cell 23(8):2950–2963. doi:10.1105/tpc.111.087973

    Article  PubMed  CAS  Google Scholar 

  • Portis AR Jr, Heldt HW (1976) Light-dependent changes of the Mg2+ concentration in the stroma in relation to the Mg2+ dependency of CO2 fixation in intact chloroplasts. Biochim Biophys Acta 449(3):434–436

    Article  PubMed  CAS  Google Scholar 

  • Potrykus K, Cashel M (2008) (p)ppGpp still magical? Annu Rev Microbiol 62:35–51. doi:10.1146/annurev.micro.62.081307.162903

    Article  PubMed  CAS  Google Scholar 

  • Pou De Crescenzo MA, Gallais S, Leon A, Laval-Martin DL (2001) Tween-20 activates and solubilizes the mitochondrial membrane-bound, calmodulin dependent NAD+ finase of Avena sativa L. J Membr Biol 182(2):135–146

    Article  PubMed  CAS  Google Scholar 

  • Reddy VS, Ali GS, Reddy ASN (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277(12):9840–9852. doi:10.1074/jbc.M111626200

    Article  PubMed  CAS  Google Scholar 

  • Roh MH, Shingles R, Cleveland MJ, McCarty RE (1998) Direct measurement of calcium transport across chloroplast inner envelope vesicles. Plant Physiol 118(4):1447–1454

    Article  PubMed  CAS  Google Scholar 

  • Rosa L (1981) The rapid activation in vitro of the chloroplast fructose 1,6-bisphosphatase followed using a new assay procedure. FEBS Lett 134(2):151–154. doi:10.1016/0014-5793(81)80589-3

    Article  CAS  Google Scholar 

  • Sai J, Johnson CH (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14(6):1279–1291. doi:10.1105/tpc.000653

    Article  PubMed  CAS  Google Scholar 

  • Sauer A, Robinson DG (1985) Calmodulin dependent NAD-kinase is associated with both the outer and inner mitochondrial membranes in maize roots. Planta 166(2):227–233

    Article  CAS  Google Scholar 

  • Schürmann P, Wolosiuk RA (1978) Studies on the regulatory properties of chloroplast fructose-1,6-bisphosphatase. Biochim Biophys Acta 522(1):130–138. doi:10.1016/0005-2744(78)90329-7

    Article  PubMed  Google Scholar 

  • Schwartz A (1985) Role of Ca and EGTA on stomatal movements in Commelina communis L. Plant Physiol 79(4):1003–1005

    Article  PubMed  CAS  Google Scholar 

  • Shutova T, Nikitina J, Deikus G, Andersson B, Klimov V, Samuelsson G (2005) Structural dynamics of the manganese-stabilizing protein-effect of pH, calcium, and manganese. Biochemistry 44(46):15182–15192. doi:10.1021/bi0512750

    Article  PubMed  CAS  Google Scholar 

  • Stael S, Bayer RG, Mehlmer N, Teige M (2011a) Protein N-acylation overrides differing targeting signals. FEBS Lett 585(3):517–522. doi:10.1016/j.febslet.2011.01.001

    Article  PubMed  CAS  Google Scholar 

  • Stael S, Rocha AG, Robinson AJ, Kmiecik P, Vothknecht UC, Teige M (2011b) Arabidopsis calcium-binding mitochondrial carrier proteins as potential facilitators of mitochondrial ATP-import and plastid SAM-import. FEBS Lett 585(24):3935–3940. doi:10.1016/j.febslet.2011.10.039

    Article  PubMed  CAS  Google Scholar 

  • Stael S, Rocha AG, Wimberger T, Anrather D, Vothknecht UC, Teige M (2011c) Crosstalk between calcium signalling and protein phosphorylation at the thylakoid membrane. J Exp Bot. doi:10.1093/jxb/err394

  • Surek B, Kreimer G, Melkonian M, Latzko E (1987) Spinach ferredoxin is a calcium-binding protein. Planta 171(4):565–568. doi:10.1007/bf00392307

    Article  CAS  Google Scholar 

  • Takahashi K, Kasai K, Ochi K (2004) Identification of the bacterial alarmone guanosine 5′-diphosphate 3′-diphosphate (ppGpp) in plants. Proc Natl Acad Sci 101(12):4320–4324. doi:10.1073/pnas.0308555101

    Article  PubMed  CAS  Google Scholar 

  • Tang R-H, Han S, Zheng H, Cook CW, Choi CS, Woerner TE, Jackson RB, Pei Z-M (2007) Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315(5817):1423–1426. doi:10.1126/science.1134457

    Article  PubMed  CAS  Google Scholar 

  • Tozawa Y, Nomura Y (2011) Signalling by the global regulatory molecule ppGpp in bacteria and chloroplasts of land plants. Plant biology 13(5):699–709. doi:10.1111/j.1438-8677.2011.00484.x

    Article  PubMed  CAS  Google Scholar 

  • Tozawa Y, Nozawa A, Kanno T, Narisawa T, Masuda S, Kasai K, Nanamiya H (2007) Calcium-activated (p)ppGpp synthetase in chloroplasts of land plants. J Biol Chem 282(49):35536–35545. doi:10.1074/jbc.M703820200

    Article  PubMed  CAS  Google Scholar 

  • Trewavas A (1999) Le calcium, C'est la vie: calcium makes waves. Plant Physiol 120(1):1–6

    Article  PubMed  CAS  Google Scholar 

  • Turner WL, Waller JC, Vanderbeld B, Snedden WA (2004) Cloning and characterization of two NAD Kinases from Arabidopsis. Identification of a calmodulin binding isoform. Plant Physiol 135(3):1243–1255. doi:10.1104/pp.104.040428

    Article  PubMed  CAS  Google Scholar 

  • Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y, Paakkarinen V, Aro E, Suorsa M, Scheller HV, Vener AV, Aro EM (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. FEBS J 275(8):1767–1777. doi:10.1111/j.1742-4658.2008.06335.x

    Article  PubMed  CAS  Google Scholar 

  • Wang W-H, Yi X-Q, Han A-D, Liu T-W, Chen J, Wu F-H, Dong X-J, He J-X, Pei Z-M, Zheng H-L (2011) Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J Exp Bot. doi:10.1093/jxb/err259

  • Weinl S, Held K, Schlücking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179(3):675–686. doi:10.1111/j.1469-8137.2008.02492.x

    Article  PubMed  CAS  Google Scholar 

  • Wolosiuk RA, Hertig CM, Nishizawa AN, Buchanan BB (1982) Enzyme regulation in C-4 photosynthesis. 3. Role of Ca2+ in thioredoxin-linked activation of sedoheptulose bisphosphatase from corn leaves. FEBS Lett 140(1):31–35

    Article  CAS  Google Scholar 

  • Yamagishi A, Satoh K, Katoh S (1981) The concentrations and thermodynamic activities of cations in intact Bryopsis chloroplasts. Biochim Biophys Acta 637(2):252–263

    Article  CAS  Google Scholar 

  • Yang T, Poovaiah BW (2000) Arabidopsis chloroplast chaperonin 10 is a calmodulin-binding protein. Biochem Biophys Res Commun 275(2):601–607. doi:10.1006/bbrc.2000.3335

    Article  PubMed  CAS  Google Scholar 

  • Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM (2005) The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J Biol Chem 280(16):16170–16174. doi:10.1074/jbc.M501550200

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work has been funded by the EU within the Marie-Curie ITN COSI (ITN 2008 GA 215-174) and by the Deutsche Forschungsgemeinschaft via ERA-NETs “Plant Genomics” (ERAPG 08-044).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ute C. Vothknecht.

Additional information

Handling Editor: David Robinson

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rocha, A.G., Vothknecht, U.C. The role of calcium in chloroplasts—an intriguing and unresolved puzzle. Protoplasma 249, 957–966 (2012). https://doi.org/10.1007/s00709-011-0373-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-011-0373-3

Keywords

Navigation