Skip to main content
Log in

External calcium requirements for light induction of chlorophyll accumulation and its enhancement by red light and cytokinin pretreatments in excised etiolated cucumber cotyledons

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Excised etiolated cucumber (Cucumis sativus L.) cotyledons that were depleted of external Ca2+ by equilibration with a Ca2+ buffer, which maintained the free Ca2+ concentration at 10−8 M, failed to accumulate chlorophyll upon a 2-h exposure to white light. Increasing amounts of chlorophyll accumulation occurred at increasing external Ca2+ concentrations within the range of 10−7-10−3 M. Preillumination with red light or pretreatment with benzyladenine, which enhanced the rate of light-induced chlorophyll accumulation in control cotyledons, did not overcome the block to light-induced chlorophyll accumulation caused by the depletion of external Ca2+. Etiolated cotyledons that were treated with the Ca2+ ionophore, A23187, and then equilibrated with 10−5 M Ca2+, accumulated significantly more chlorophyll during exposure to light than did untreated cotyledons. The enhancing effect of A23187 was approximately equal to that caused by red-light pretreatment. Etiolated cotyledons that were exposed to the Ca2+ channel-blocking agent, Nd3+ (neodymium), in the presence of 10−5 M Ca2+, did not exhibit an enhancement of chlorophyll accumulation by red-light pretreatment, although they accumulated control levels of chlorophyll upon exposure to light and showed control levels of enhancement of chlorophyll accumulation by cytokinin pretreatment. Conversely, etiolated cotyledons that were equilibrated with 10−5 M Ca2+ in the presence of nifedipine, a blocker of some Ca2+ channels, did not exhibit an enhancement of chlorophyll accumulation by cytokinin pretreatment, although they accumulated control levels of chlorophyll upon exposure to light and showed control levels of enhancement of chlorophyll accumulation by red-light pretreatment. These results indicate that external Ca2+ is required for chlorophyll accumulation by excised etiolated cucumber cotyledons during the first 2 h of light exposure, and that an influx of external Ca2+ is required for the enhancing effect of redlight and cytokinin. The differential abilities of Nd3+ and nifedipine to block the effects of red-light and cytokinin pretreatments suggests that enhancement of chlorophyll accumulation by red-light and cytokinin may involve different classes of Ca2+ channels.

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.

Similar content being viewed by others

Abbreviations

A23187:

antibiotic 23187 calcium ionophore

Chl:

chlorophyll

nifedipine:

1,4-dihydro-2,6-dimethyl-4-(2′-nitrophenyl)-3,5-pyridinedicarboxylic acid dimethyl ester

References

  • Appenroth, K.-J., Dürr, S., Gabryś, H., Scheuerlein, R. (1994) No regulation of45calcium-uptake or release by phytochrome as an essential step in the transduction chain. Plant Physiol. Biochem.32, 429–435

    Google Scholar 

  • Beale, S.I., Castelfranco, P.A. (1974) The biosynthesis of δ- aminolevulinic acid in higher plants. I. Accumulation of δ- aminolevulinic acid in greening plant tissues. Plant Physiol.53, 291–296

    Google Scholar 

  • Beevers, L., Loveys, B., Pearson, J.A., Wareing, P.F. (1970) Phytochrome and hormonal control of expansion and greening of etiolated wheat leaves. Planta90, 286–294

    Google Scholar 

  • Bennett, J., Jenkins, G.I., Hartley, M.R. (1984) Differential regulation of the accumulation of the light-harvesting chlorophylla/b complex and ribulose bisphosphate carboxylase/oxygenase in greening pea leaves. J. Cell. Biochem.25, 1–13

    Google Scholar 

  • Bowler, C., Neuhaus, G., Yamagata, H., Chua, N.-H. (1994) Cyclic GMP and calcium mediate phytochrome phototransduction. Cell77, 73–81

    Google Scholar 

  • Briggs, W.R., Mösinger, E., Schäfer, E. (1988) Phytochrome regulation of greening in barley — effects on chlorophyll accumulation. Plant Physiol.86, 435–440

    Google Scholar 

  • Conrad, P.A., Hepler, P.K. (1988) The effect of 1,4-dihydropyridines on the initiation and development of gametophore buds in the mossFunaria. Plant Physiol.86, 684–687

    Google Scholar 

  • De Greef, J.A., Caubergs, R. (1972) Studies on greening of etiolated seedlings. I. Elimination of the lag phase of chlorophyll biosynthesis by a pre-illumination of the embryonic axis in intact plants. Physiol. Plant.26, 157–165

    Google Scholar 

  • Dei, M. (1982) A two-fold action of benzyladenine on chlorophyll formation in etiolated cucumber cotyledons. Physiol. Plant.56, 407–414

    Google Scholar 

  • Dei, M. (1985) Benzyladenine-induced stimulation of 5- aminolevulinic acid accumulation under various light intensities in levulinic acid-treated cotyledons of etiolated cucumber. Physiol Plant64, 153–160

    Google Scholar 

  • Dei, M., Tsuji, H. (1978) The influence of various plant hormones on the stimulatory action of red light on greening in excised etiolated cotyledons of cucumber. Plant Cell Physiol.19, 1407–1414

    Google Scholar 

  • Fletcher, R.A., McCullagh, D. (1971) Benzyladenine as a regulator of chlorophyll synthesis in cucumber cotyledons. Can. J. Bot.49, 2197–2201

    Google Scholar 

  • Fletcher, R.A., Teo, C., Ali, A. (1973) Stimulation of chlorophyll synthesis in cucumber cotyledons by benzyladenine. Can. J. Bot.51, 937–939

    Google Scholar 

  • Griffiths, W.T. (1978) Reconstitution of chlorophyllide formation by isolated etioplast membranes. Biochem. J.174, 681–692

    Google Scholar 

  • Hardy, S.I., Castelfranco, P.A., Rebeiz, C.A. (1970) Effect of the hypocotyl hook on greening in etiolated cucumber cotyledons. Plant Physiol.46, 705–707

    Google Scholar 

  • Hardy, S.I., Castelfranco, P.A., Rebeiz, C.A. (1971) Effect of the hypocotyl hook on chlorophyll accumulation in etiolated cotyledons ofCucumis sativus L. Plant Physiol.47, 705–708

    Google Scholar 

  • Hepler, P.K., Wayne, R.O. (1985) Calcium and plant development. Annu. Rev. Plant Physiol.36, 397–439

    Google Scholar 

  • Huang, L., Bonner, B., Castelfranco, P.A. (1989) Regulation of 5- aminolevulinic acid (ALA) synthesis in developing chloroplasts. II. Regulation of ALA-synthesizing capacity by phytochrome. Plant Physiol.90, 1003–1008

    Google Scholar 

  • Janis, R.A., Triggle, D.J. (1983) New developments in Ca2+ channel antagonists. J. Med. Chem.26, 775–785

    Google Scholar 

  • Kim, J., Eichacker, L.A., Rudiger, W., Mullet, J.E. (1994) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll proteins P700 and D1 by increasing apoprotein stability. Plant Physiol.104, 907–916

    Google Scholar 

  • Klein, R.R., Mullet, J.E. (1986) Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast biogenesis. J. Biol. Chem.261, 11138–11145

    Google Scholar 

  • Knight, M.R., Campbell, A.K., Smith, S.M., Trewavas, A.J. (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature352, 524–526

    Google Scholar 

  • Koski, V.M., French, C.S., Smith, J.H.C. (1951) The action spectrum for the transformation of protochlorophyll to chlorophylla in normal and albino corn seedlings. Arch. Biochem. Biophys.31, 1–17

    Google Scholar 

  • Lam, E., Benedyk, M., Chua, N.-H. (1989) Characterization of phytochrome-regulated gene expression in a photoautotrophic cell suspension: possible role for calmodulin. Mol. Cell. Biol.9, 4819–4823

    Google Scholar 

  • Lansman, J.B. (1990) Blockade of current through single calcium channels by trivalent lanthanide cations. J. Gen. Physiol.95, 679–696

    Google Scholar 

  • Lew, R., Tsuji, H. (1982) Effect of benzyladenine treatment duration on δ-aminolevulinic acid accumulation in the dark, chlorophyll lag phase abolition, and long-term chlorophyll production in excised cotyledons of dark-grown cucumber seedlings. Plant Physiol.69, 663–667

    Google Scholar 

  • Masoner, M., Kasemir, H. (1975) Control of chlorophyll synthesis by phytochrome. I. The effect of phytochrome on the formation of 5-aminolevulinate in mustard seedlings. Planta126, 111–117

    Google Scholar 

  • Mösinger, E., Batschauer, A., Apel, K., Schäfer, E., Briggs, W.R. (1988) Phytochrome regulation of greening in barley: effects on mRNA abundance and on transcriptional activity of isolated nuclei. Plant Physiol.86, 706–710

    Google Scholar 

  • Neuhaus, G., Bowler, C., Kern, R., Chua, N.-H. (1993) Calcium/calmodulin-dependent and-independent phytochrome signal transduction pathways. Cell73, 937–952

    Google Scholar 

  • Oelze-Karow, H., Rösch, H., Mohr, H. (1983) Prevention by phytochrome of photodelay in chlorophyll accumulation. Photochem. Photobiol.37, 565–569

    Google Scholar 

  • Reed, P.W., Lardy, H.A. (1972) A23187: a divalent cation ionophore. J. Biol. Chem.247, 6970–6977

    Google Scholar 

  • Reiss, C., Wayne, R. (1989) The effect of Ca2+ on chlorophyll synthesis in cucumber (Cucumis sativa) cotyledons. (Abstr.) Plant Physiol.89, Suppl., 21

    Google Scholar 

  • Reiss, C., Wayne, R. (1990) The effect of Ca2+ on cytokinin enhanced chlorophyll accumulation. (Abstr.) Plant Physiol.93, Suppl., 127

    Google Scholar 

  • Roux, S.J. (1984) Ca2+ and phytochrome action in plants. Bioscience34, 25–29

    Google Scholar 

  • Saunders, M.J., Hepler, P.K. (1983) Calcium antagonists and calmodulin inhibitors block cytokinin-induced bud formation inFunaria. Dev. Biol.99, 41–49

    Google Scholar 

  • Staves, M.P., Wayne, R. (1993) The touch-induced action potential inChara: inquiry into the ionic basis and the mechanoreceptor. Aust. J. Plant Physiol.20, 471–488

    Google Scholar 

  • Tew, W.P. (1977) Use of coulombic interactions of the lanthanide series to identify two classes of Ca2+ binding sites in mitochondria. Biochem. Biophys. Res. Commun.78, 624–630

    Google Scholar 

  • Tretyn, A., Kendrick, R.E., Wagner, G. (1991) The role(s) of calcium ions in phytochrome action. Photochem. Photobiol.54, 1135–1155

    Google Scholar 

  • Tsien, R.W., Hess, P., McCleskey, E.W., Rosenberg, R.L. (1987) Calcium channels: mechanisms of selectivity, permeation, and block. Annu. Rev. Biophys. Chem.16, 265–290

    Google Scholar 

  • Virgin, H.I. (1955) Protochlorophyll formation and greening in etiolated barley leaves. Physiol. Plant.8, 630–643

    Google Scholar 

  • Virgin, H.I. (1961) Action spectrum for the elimination of the lag phase in chlorophyll formation in previously dark grown leaves of wheat. Physiol. Plant.14, 439–452

    Google Scholar 

  • Wayne, R. (1985) The contribution of calcium ions and hydrogen ions to the signal transduction chain in phytochrome-mediated spore germination. Ph.D. thesis, University of Massachusetts, Amherst, USA

    Google Scholar 

  • Wehmeyer, B., Cashmore, A.R., Schäfer, E. (1990) Photocontrol of expression of genes encoding chlorophyll a/b binding proteins and small subunit of ribulose-1,5-bisphosphate carboxylase in etiolated seedlings ofLycopersicon esculentum (L.) andNicotiana tabacum (L.). Plant Physiol.93, 990–997

    Google Scholar 

  • Zhao, Z., Ross, C.W. (1989) Effects of compounds that influence calcium absorption and of calcium-calmodulin inhibitors on zeatin induced growth and chlorophyll synthesis in excised cucumber cotyledons. Plant Cell Physiol.30, 793–800

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carol Reiss.

Additional information

We thank Randy Wayne for advice and encouragement.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reiss, C., Beale, S.I. External calcium requirements for light induction of chlorophyll accumulation and its enhancement by red light and cytokinin pretreatments in excised etiolated cucumber cotyledons. Planta 196, 635–641 (1995). https://doi.org/10.1007/BF01106754

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01106754

Key words

Navigation