Abstract
Tracheary-element (TE) differentiation in suspension cultures ofZinnia elegans L. mesophyll cells was inhibited by blocking calcium uptake in three ways: 1) reducing the [Ca2+] of the culture medium, 2) blocking calcium channels with the non-permeant cation La3+, and 3) blocking calcium channels with permeant dihydropyridine calcium-channel blockers. Calcium-channel blockers were effective when added at any time between 0 and 48 h after culture initiation; after 48h, calcium sequestration and secondary cell-wall deposition began. In contrast, calmodulin antagonists inhibited TE differentiation when added at the beginning of culture, but not when added after 24h. These results indicate that TE differentiation involves at least two calcium-regulated events: one calmodulin-dependent and occurring shortly after exposure to inductive conditions, and the other calmodulin-independent and occurring just prior to secondary cell-wall deposition.
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Abbreviations
- BA:
-
N6-benzylaminopurine
- CPZ:
-
chlorpromazine
- DIC:
-
differential interference contrast
- DMSO:
-
dimethylsulfoxide
- IC50 :
-
concentration resulting in 50% inhibition
- TE:
-
tracheary element
- TFP:
-
trifluoperazine
- W-5:
-
N-(6-aminohexyl)-1-naphthylenesulfonamide
- W-7:
-
N-(6-aminohexyl)-5-chloro-1-naphthylenesulfonamide
References
Asano, M., Hidaka, H. (1984) Biopharmacological properties of naphthalenesulfonamides as potent calmodulin antagonists. In: Calcium and cell function, vol. 5, pp. 123–164, Cheung, W.Y., ed. Academic Press, New York
Church, D.L., Galston, A.W. (1988) Kinetics of determination in the differentiation of isolated mesophyll cells ofZinnia elegans to tracheary elements. Plant Physiol.88, 92–96
Dörrscheidt-Käfer, M. (1977) The action of D600 on frog skeletal muscle: facilitation of excitation-contraction coupling. Pflügers Arch.369, 259–267
dos Remedios, C.G. (1981) Lanthanide ion probes of calcium-binding sites on cellular membranes. Cell Calcium2, 29–51
Elliott, D.C. (1983) Inhibition of cytokinin-regulated responses by calmodulin binding compounds. Plant Physiol.72, 215–218
Falconer, M.M., Seagull, R.W. (1985) Xylogenesis in tissue culture: taxol effects on microtubule reorientation and lateral association in differentiating cells. Protoplasma128, 157–166
Fukuda, H., Komamine, A. (1980a) Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll ofZinnia elegans. Plant Physiol.65, 57–60
Fukuda, H., Komamine, A. (1980b) Direct evidence for cytodifferentiation to tracheary elements without intervening mitosis in culture of single cells isolated from the mesophyll ofZinnia elegans. Plant Physiol.65, 61–64
Fukuda, H., Komamine, A. (1985) Cytodifferentiation. In: Cell culture and somatic cell genetics of plants, vol. 2. pp. 149–211, Vasil, I.K., ed., Academic Press, New York
Haigler, C.H., Brown, R.M., Jr. (1986) Transport of rosettes from the Golgi apparatus to the plasma membrane in isolated mesophyll cells ofZinnia elegans during differentiation to tracheary elements in suspension culture. Protoplasma134, 111–120
Hepler, P.K. (1985) Calcium restriction prolongs metaphase in dividingTradescantia stamen hair cells. J. Cell Biol.100, 1363–1368
Hepler, P.K., Wayne, R.O. (1985) Calcium and plant development. Annu. Rev. Plant Physiol.36, 397–439
Hescheler, J., Pelzer, D., Trube, B., Trautwein, W. (1982) Does the organic calcium channel blocker D600 act from inside or outside on the cardiac cell membrane? Pflugers Arch.393, 287–291
Hille, B. (1984) Ionic channels of excitable membranes. Sinauer Associates, Inc., Sunderland, Mass., USA
Hof, R.P., Ruegg, U.T., Hof, A., Vogel, A. (1985) Stereoselectivity at the calcium channel: opposite action of the enantiomers of a 1,4-dihydropyridine. J. Cardiovasc. Pharmacol.7, 689–693
Hosey, M.M., Lazdunski, M. (1988) Calcium channels: molecular pharmacology, structure and regulation. J. Membr. Biol.104, 81–105
Ingold, E., Sugiyama, M., Komamine, A. (1988) Secondary cell wall formation: changes in cell wall constituents during the differentiation of isolated mesophyll cells ofZinnia elegans to tracheary elements. Plant Cell Physiol.29, 295–303
Kass, R.S., Arena, J.P., (1989) Influence of pH0 on calcium channel block by amlodipine, a charged dihydropyridine compound. Implications for location of the dihydropyridine receptor. J. Gen. Physiol.93, 1109–1127
Lehtonen, J. (1984) The significance of Ca2+ in the morphogenesis ofMicrasterias studied with EGTA, verapamil, LaCl3 and calcium ionophore A 23187. Plant Sci. Lett.33, 53–60
Moore, P.B., Dedman, J.R. (1982) Calcium-dependent protein binding to phenothiazine columns. J. Biol. Chem.257, 9663–9667
Morad, M., Goldman, Y.E., Trentham, D.R. (1983) Rapid photochemical inactivation of Ca2+-antagonist shows that Ca2+ entry directly activates contraction in frog heart. Nature304, 635–638
Murashige, T., Skoog, F., (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant.15, 473–497
Phillips, R. (1987) Effects of sequential exposure to auxin and cytokinin on xylogenesis in cultured explants of Jerusalem artichoke (Helianthus tuberosus L.). Ann. Bot.59, 245–250
Prozialek, W.C., Weiss, B. (1982) Inhibition of calmodulin by phenothiazines and related drugs: structure-activity relationships. J. Pharmacol. Exp. Ther.222, 509–516
Roberts, A.W., Haigler, C.H. (1989) Rise in chlorotetracycline fluorescence accompanies tracheary element differentiation in suspension cultures ofZinnia. Protoplasma152, 37–45
Roberts, L.W., Baba, S. (1987) Evidence that auxin-induced xylogenesis inLactuca explants requires calmodulin. Environ. Exp. Bot.27, 289–295
Roufogalis, B.D. (1985) Calmodulin antagonism. In: Calcium and cell physiology, pp. 148–169, Marmé, D., ed. Springer, New York Heidelberg Berlin
Ruth, J.B., Kotenko, J.L., Miller, J.H. (1988) Role of asymmetric cell division in pteridophyte differentiation. II. Effect of Ca2+ on asymmetric cell division, rhizoid elongation, and antheridium differentiation inVittaria gemmae. Am. J. Bot.75, 1755–1764
Saunders, M.J. (1986) Cytokinin activation and redistribution of plasma-membrane ion channels inFunaria. A vibrating-micro-electrode and cytoskeleton-inhibitor study. Planta167, 402–409
Saunders, M.J., Hepler, P.K. (1983) Calcium antagonists and calmodulin inhibitors block cytokinin-induced bud formation inFunaria. Dev. Biol.99, 41–49
Steer, M.W. (1988) The role of calcium in exocytosis and endocytosis in plant cells. Physiol. Plant.72, 213–220
Tanimoto, S., Harada, H. (1986) Involvement of calcium in adventitious bud initiation inTorenia stem segments. Plant Cell Physiol.27, 1–10
Thomson, W.W., Platt, K.A., Campbell, N. (1973) The use of lanthanum to delineate the apoplastic continuum in plants. Cytobios8, 57–62
Triggle, C.R. (1980) Site of action of D-600 in guinea-pig ileal longitudinal muscle. J. Physiol.305, 82P
Tucker, W.Q.J., Wilson, J.W., Gresshoff, P.M. (1986) Determination of tracheary element differentiation in lettuce pith explants. Ann. Bot.57, 675–679
Uehara, A., Hume, J.R. (1985) Interactions of organic calcium channel antagonists with calcium channels in single frog atrial cells. J. Gen. Physiol.85, 621–647
Wolniak, S.M., Bart, K.M. (1985) Nifedipine reversibly arrests mitosis in stamen hair cells ofTradescantia. Eur. J. Cell Biol.39, 273–277
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Roberts, A.W., Haigler, C.H. Tracheary-element differentiation in suspension-cultured cells ofZinnia requires uptake of extracellular Ca2+ . Planta 180, 502–509 (1990). https://doi.org/10.1007/BF02411447
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DOI: https://doi.org/10.1007/BF02411447