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Regulation and Role of Calcium Fluxes in the Chloroplast

  • Carl Hirschie Johnson
  • Richard Shingles
  • William F. Ettinger
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 23)

Ionized free calcium (Ca++) is a crucial-and practically ubiquitous-regulator of biological processes. There is much information about the regulation of cytosolic Ca++ levels and fluxes in plants, but very little is known about its regulation in the chloroplast, despite clear evidence for the importance of calcium in this organelle. The chloroplast contains calcium-binding proteins, such as calmodulin, calcium-regulated kinases, and calcium transport proteins.

Keywords

Thylakoid Membrane Envelope Membrane Intact Chloroplast Thylakoid Lumen Chloroplast Stroma 
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.

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References

  1. Anderson JM, Charbonneau H, Jones HP, McCann RO and Cormier MJ (1980) Characterization of the plant nicotinamide adenine dinucleotide kinase activator protein and its identification as calmodulin. Biochemistry 19: 3113-3120CrossRefPubMedGoogle Scholar
  2. Baum G, Long JC, Jenkins GI and Trewavas AJ (1999) Stim-ulation of the blue light phototropic receptor NPH1 causes transient increase in cytosolic Ca++ . Proc Natl Acad Sci USA 96: 13554-13559CrossRefPubMedGoogle Scholar
  3. Becker DW, Callahan FE and Cheniae GM (1985) Photoactiva-tion of NH2 OH-treated leaves: reassembly of released extrin-sic PSII polypeptides and religation of Mn into the polynuclear Mn catalyst of water oxidation. FEBS Lett 192: 209-214CrossRefGoogle Scholar
  4. Blackford S, Rea PA and Sanders D (1990) Voltage sensitivity of H+ /Ca2+ antiport in higher plant tonoplast suggests a role in vacuolar calcium accumulation. J Biol Chem 265: 9617-9620PubMedGoogle Scholar
  5. Bolter B and Soll J (2001) Ion channels in the outer membranes of chloroplasts and mitochondria: open doors or regulated gates. The EMBO Journal 20: 935-940CrossRefPubMedGoogle Scholar
  6. Broussac A, Zimmermann J-L, Rutherford AW and Lavergne J (1990) Histidine oxidation in the oxygen-evolving photosys-tem II enzyme. Nature 347: 303-306CrossRefGoogle Scholar
  7. Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46: 95-122CrossRefGoogle Scholar
  8. Cheng S-H, Willman MR, Chen H-C and Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129: 469-485CrossRefPubMedGoogle Scholar
  9. Cheng N-H, Pittman JK, Zhu J-K and Hirschi KD (2004) The protein kinase SOS2 activates the Arabidopsis Ca++ /H+ an-tiporter CAX1 to integrate calcium transport and salt toler-ance. J Biol Chem 279: 2922-2926CrossRefPubMedGoogle Scholar
  10. Debus RJ (1992) The manganese and calcium ions of photosyn-thetic oxygen evolution. Biochim Biophys Acta 1102: 269-352CrossRefPubMedGoogle Scholar
  11. Demmig B and Gimmler H (1979) Effect of divalent cations on cation fluxes across the chloroplast envelope and on photosyn-thesis of intact chloroplasts. Z Naturforsch 34c: 233-241Google Scholar
  12. Emanuelsson O, Nielsen H, Brunak S and von Heijne G (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016CrossRefPubMedGoogle Scholar
  13. Ettinger WF, Clear AM, Fanning KJ and Peck ML (1999) Identifi-cation of a Ca++ /H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119: 1379-1385CrossRefPubMedGoogle Scholar
  14. Evans DE, Briars SA and Williams LE (1991) Active Ca++ trans-port by plant cell membranes. J Exp Bot 42: 285-303CrossRefGoogle Scholar
  15. Flugge UI and Benz R (1984) Pore forming activity in the outer membrane of the chloroplast envelope. FEBS Lett 169: 85-89CrossRefGoogle Scholar
  16. Frohnmeyer H, Loyall L, Blatt MR and Grabov A (1999) A millisecond UV-B irradiation evokes prolonged elevation of cytosolic-free Ca++ and stimulates gene expression in trans-genic parsley cell cultures. Plant J 20: 109-117CrossRefPubMedGoogle Scholar
  17. Ghanotakis DF, Babcock GT and Yocum CF (1984) Calcium reconstitutes high levels of oxygen evolution in polypeptide-depleted photosystem II preparations. FEBS Lett 167: 127-130.CrossRefGoogle Scholar
  18. Grove GN and Brudvig GW (1998) Calcium binding studies of photosystem II using a calcium-selective electrode. Biochem-istry 37: 1532-1539CrossRefGoogle Scholar
  19. Heldt HW, Werdan K, Milovancev M and Geller G (1973) Alka-linization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochem Biophys Acta 314: 224-241CrossRefPubMedGoogle Scholar
  20. Hertig CM and Wolosiuk RA (1983) Studies on the hysteretic properties of chloroplast fructose-1,6-bisphosphatase. J Biol Chem 258: 984-989PubMedGoogle Scholar
  21. Hetherington AM and Trewavas A (1982) Calcium-dependent protein kinase in pea shoot membranes. FEBS Lett 145: 67-71CrossRefGoogle Scholar
  22. Hirschi KD, Zhen R-G, Cunningham KW, Rea PA and Fink GR (1996) CAX1: an H+ /Ca2+ antiporter from Arabidopsis. Proc Natl Acad Sci USA 93: 8782-8786CrossRefPubMedGoogle Scholar
  23. Huang L, Berkelman T, Franklin AE and Hoffman NE (1993) Characterization of a gene encoding a Ca++ -ATPase-like pro-tein in the plastid envelope. Proc Natl Acad Sci USA 90: 10066-10070CrossRefPubMedGoogle Scholar
  24. Hundal T, Aro EM, Carlberg I and Andersson B (1990a) Restora-tion of light induced photosystem II inhibition without de novo protein synthesis. FEBS Lett 267: 203-206CrossRefGoogle Scholar
  25. Hundal T, Virgin I, Styring S and Andersson B (1990b) Changes in the organization of photosystem II following light-induced D1 protein degradation. Biochem Biophys Acta 1017: 235-241CrossRefGoogle Scholar
  26. Jarrett HW, Brown CJ, Black CC and Cormier MJ (1982) Evi-dence that calmodulin is in the chloroplast of peas and serves a regulatory role in photosynthesis. J Biol Chem 257: 13795-13804PubMedGoogle Scholar
  27. Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A and Trewavas AJ (1995) Circadian oscillations of cytosolic and chloroplastidic free calcium in plants. Science 269: 1863-1865CrossRefPubMedGoogle Scholar
  28. Knight MR, Campbell AK, Smith SM and Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352: 524-526CrossRefPubMedGoogle Scholar
  29. Kramer DM and Crofts AR (1989) Activation of the chloroplast ATPase measured by the electrochromic change in leaves of intact plants. Biochim Biophys Acta 976: 28-41CrossRefGoogle Scholar
  30. Kreimer G, Melkonian M, Holtum JAM and Latzko E (1985a) Characterization of calcium fluxes across the envelope of intact spinach chloroplasts. Planta 166: 515-523CrossRefGoogle Scholar
  31. Kreimer G, Melkonian M and Latzko E (1985b) An electro-genic uniport mediates light-dependent Ca++ influx into intact spinach chloroplasts. FEBS Lett 180: 253-258CrossRefGoogle Scholar
  32. Kreimer G, Surek B, Woodrow IE and Latzko E (1987) Calcium binding by spinach stromal proteins. Planta 171: 259-265CrossRefGoogle Scholar
  33. Kreimer G, Melkonian M, Holtum JAM and Latzko E (1988) Stromal free calcium concentration and light-mediated activa-tion of chloroplast fructose-1,6-bisphosphatase. Plant Physiol 86: 423-428CrossRefPubMedGoogle Scholar
  34. Leng Q, Mercier RW, Yao WZ and Berkowitz GA (1999) Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol 121:753-761CrossRefPubMedGoogle Scholar
  35. Li CF, Xiang ZY, Ling QL and Shang KJ (1998) Effects of calmodulin and calmodulin binding protein BP-10 on phos-phorylation of thylakoid membrane protein. Sci China Ser C-Life Sci 41: 64-70CrossRefGoogle Scholar
  36. Malmstrom S, Askerlund P and Palmgren MG (1997) A calmodulin-stimulated Ca++ - ATPase from plant vacuo-lar membranes with a putative regulatory domain at its N-terminus. FEBS Lett 400: 324-328CrossRefPubMedGoogle Scholar
  37. M äser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA and Guerinot ML. (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126: 1646-67CrossRefGoogle Scholar
  38. Mattoo AK, Marder JB and Edelman M (1989) Dynamics of the photosystem II reaction center. Cell 56: 241-246CrossRefPubMedGoogle Scholar
  39. McAinsh MR and Hetherington AM (1998) Encoding specificity in Ca++ signaling systems. Trends Plant Sci 3: 32-36CrossRefGoogle Scholar
  40. McNamera VP and Gounaris K (1995) Granal photosystem II complexes contain only the high redox potential form of cy-tochrome b-559 which is stabilized by the ligation of calcium. Biochem Biophys Acta 1231: 289-296CrossRefGoogle Scholar
  41. Melkonian B, Burchert M, Kreimer G and Latzko E (1990) Bind-ing and possible function of calcium in the chloroplast. Curr Top Plant Biochem Physiol 9: 38-46Google Scholar
  42. Millar AJ, McGrath RB and N-H Chua (1994) Phytochrome pho-totransduction pathways. Annu Rev Genet 28: 325-349CrossRefPubMedGoogle Scholar
  43. Miller A-F and Brudvig GW (1989) Manganese and calcium requirements for reconstitution of oxygen-evolution activity in manganese-depleted photosystem II membranes. Biochem-istry 28: 8181-8190CrossRefGoogle Scholar
  44. Miller AJ and Sanders D (1987) Depletion of cytosolic free cal-cium induced by photosynthesis. Nature 326: 397-400CrossRefGoogle Scholar
  45. Muto S and Miyachi S (1977) Properties of a protein activator of NAD kinase from plants. Plant Physiol 59: 55-60CrossRefPubMedGoogle Scholar
  46. Muto S, Miyachi S, Usuda H, Edwards GE and Bassham JA (1981) Light-induced conversion of nicotinamide adenine din-ucleotide to nicotinamide adenine dinucleotide phosphate in higher plant leaves. Plant Physiol 68: 324-328CrossRefPubMedGoogle Scholar
  47. Muto S, Izawa S and Miyachi S (1982) Light-induced Ca++ uptake by intact chloroplasts. FEBS Lett 139: 250-254CrossRefGoogle Scholar
  48. Nakai K and Horton P (1999) PSORT: a program for detecting the sorting signals of proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-35CrossRefPubMedGoogle Scholar
  49. Navazio L, Bewell MA, Siddiqua A, Dickinson GD, Galione A and Sanders D (2000) Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate. Proc Natl Acad Sci USA 97: 8693-8698CrossRefPubMedGoogle Scholar
  50. Pittman JK and Hirschi KD (2001) Regulation of CAX1, an Ara-bidopsis Ca2+ /H+ antiporter. Identification of an N-terminal autoinhibitory domain. Plant Physiol 127: 1020-1029CrossRefPubMedGoogle Scholar
  51. Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H and Hirschi KD (2002) Distinct N-terminal regulatory domains of Ca2+ /H+ antiporters. Plant Physiol 130: 1054-1062CrossRefPubMedGoogle Scholar
  52. Pohlmeyer K, Soll J, Grimm R, Hill K and Wagner R (1998) A high-conductance solute channel in the chloroplastic outer envelope from pea. Plant Cell 10: 1207-1216CrossRefPubMedGoogle Scholar
  53. Portis AR Jr and Heldt HW (1976) Light-dependent changes of the Mg++ concentration in the stroma in relation to the Mg++ dependency of CO2 fixation in intact chloroplasts. Biochim Biophys Acta 449: 434-446CrossRefPubMedGoogle Scholar
  54. Roberts DM and Harmon AC (1992) Calcium-modulated pro-teins: targets of intracellular calcium signals in higher plants. Annu Rev Plant Physiol Plant Mol Biol 43: 375-414CrossRefGoogle Scholar
  55. Roh MH, Shingles R, Cleveland MJ and McCarty RE (1998) Direct measurement of calcium transport across chloroplast inner-envelope vesicles. Plant Physiol 118: 1447-1454.CrossRefPubMedGoogle Scholar
  56. Sai J and Johnson CH (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14: 1279-1291CrossRefPubMedGoogle Scholar
  57. Sanders D, Brownlee C and Harper JF (1999) Communicating with calcium. Plant Cell 11: 691-706CrossRefPubMedGoogle Scholar
  58. Sanders D, Pelloux J, Brownlee C and Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14: S401-S417PubMedGoogle Scholar
  59. Schuldiner S, Rottenberg H and Avron M (1972) Determination of pH in chloroplasts. 2. Fluorescent amines as a probe for the determination of pH in chloroplasts. Eur J Biochem 25: 64-70CrossRefPubMedGoogle Scholar
  60. Schwacke R, Schneider A, van der Graff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flugge UI and Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131: 16-26.CrossRefPubMedGoogle Scholar
  61. Shaul O, Hilgemann DW, de-Almeida-Engler J, Van Montagu M, Inz D and Galili G (1999) Cloning and characterization of a novel Mg2+ /H+ exchanger. EMBO J 18: 3973-3980CrossRefPubMedGoogle Scholar
  62. Shingles R and McCarty RE (1995) Production of mem-brane vesicles by extrusion: size distribution, enzyme activity, and orientation of plasma membrane and chloroplast inner-envelope membrane vesicles. Anal Biochem 229: 92-98CrossRefPubMedGoogle Scholar
  63. Trewavas AJ and Malho R (1997) Signal perception and trans-duction: the origin of the phenotype. Plant Cell 9: 1181-1195CrossRefPubMedGoogle Scholar
  64. Ueoka-Nakanishi H, Tsuchiya T, Sasaki M, Nakanishi Y, Cun-ninghamm KW and Maeshima M (2000) Functional expres-sion of mung bean Ca++ /H+ antiporter in yeast and its in-tracellular localization in hypocotyls and tobacco cells. Eur J Biochem 267: 3090-3098CrossRefPubMedGoogle Scholar
  65. Vander Meulen KA, Hobson A and Yocum CF (2002) Calcium depletion modifies the structure of the photosystem II O2 -evolving complex. Biochemistry 41: 958-66CrossRefPubMedGoogle Scholar
  66. Virgin I, Ghanotakis DF and Andersson B (1990) Light induced D1-protein degradation in isolated photosystem II core com-plexes. FEBS Lett 269: 45-48CrossRefPubMedGoogle Scholar
  67. Vrettos JS, Stone DA and Brudvig GW (2001) Quantifying the ion selectivity of the Ca2+site in photosystem II: evidence for direct involvement of Ca2+in O2 formation. Biochemistry 40: 7937-7945CrossRefPubMedGoogle Scholar
  68. Wolosiuk RA, Ballicora MA and Hagelin K (1993) The reductive pentose phosphate cycle for photosynthetic CO2 assimilation: enzyme modulation. FASEB J 7: 622-737PubMedGoogle Scholar
  69. Wu Y, Kuzma J, Mar échal E, Graeff R, Lee HC, Foster R and Chua N-H (1997) Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278: 2126-2130CrossRefPubMedGoogle Scholar
  70. Yang T and Poovaiah BW (2000) Arabidopsis chloroplast chap-eronin 10 is a calmodulin-binding protein. Biochem Biophys Res Commun 275: 601-607CrossRefPubMedGoogle Scholar
  71. Zhang L and Lu Y-T (2003) Calmodulin-binding protein kinases in plants. Trends Plant Sci 8: 123-127CrossRefPubMedGoogle Scholar
  72. Zielinski RE (1998) Calmodulin and calmodulin-binding pro-teins in plants. Annu Rev Plant Physiol Plant Mol Biol 49: 697-725CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Carl Hirschie Johnson
    • 1
  • Richard Shingles
    • 2
  • William F. Ettinger
    • 3
  1. 1.Department of Biological SciencesVanderbilt UniversityNashvilleUSA
  2. 2.Department of BiologyJohns Hopkins UniversityBaltimoreUSA
  3. 3.Biology DepartmentGonzaga UniversitySpokaneUSA

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