Abstract
RECENT investigations suggest that cytoplasmic D-myo-inositol 1,4,5-trisphosphate (InsP3) functions as a second messenger in plants, as in animals, coupling environmental and other stimuli to intracellular Ca2+ release1,2. Cytoplasmic levels of InsP3 and the turnover of several probable precursors in plants are affected by physiological stimuli—including light, osmotic stress and the phytohormone indoleacetic acid3–5—and InsP3 activates Ca2+ channels6 and Ca2+ flux across plant vacuolar7 and microsomal membranes8. Complementary data also link changes in cytoplasmic free Ca2+ to several physiological responses, notably in guard cells which regulate gas exchange through the stomatal pores of higher plant leaves. Recent evidence indicates that guard cell K+ channels and, hence, K+ flux for stomatal movements9 may be controlled by cytoplasmic Ca2+ (ref. 10). So far, however, direct evidence of a role for InsP3 in signalling in plants has remained elusive. Here we report that InsP3 released from an inactive, photolabile precursor, the P5-l-(2-nitrophenyl)ethyl ester of InsP3 (caged InsP3)11 reversibly inactivates K+ channels thought to mediate K+ uptake by guard cells from Vicia faba L. while simultaneously activating an apparently time-independent, inward current to depolarize the membrane potential and promote K+ efflux through a second class of K+ channels12,13. The data are consistent with a transient rise in cytoplasmic free Ca2+ (ref. 9) and demonstrate that intact guard cells are competent to use InsP3 in signal cascades controlling ion flux through K+ channels.
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References
Berridge, M. J. & Irvine, R. F. Nature 341, 197–202 (1989).
Thiel, G., MacRobbie, E. A. C. & Hanke, D. EMBO J. 9, 1737–1741 (1990).
Morse, M. J., Crain, R. C. & Satter, R. L. Proc. natn. Acad. Sci. U.S.A. 84, 7075–7078 (1987).
Ettlinger, C. & Lehle, L. Nature 331, 176–178 (1988).
Srivastrava, A., Pines, M. & Jacoby, B. Physiol. Pl. 77, 320–325 (1989).
Alexandre, J., Lassalles, J. P. & Kado, R. T. Nature 343, 567–570 (1990).
Ranjeva, R., Carrasco, A. & Boudet, A. M. FEBS Lett. 230, 137–141 (1988).
Drøbak, B. K. & Ferguson, I. B. Biochem. Biophys. Res. Commun. 130, 1241–1246 (1985).
Schroeder, J. I. & Hagiwara, S. Nature 338, 427–430 (1989).
McAinsh, m. R., Brownless, C. & Hetherington, A. M. Nature 343, 186–188 (1990).
Walker, J. W., Feeney, J. & Trentham, D. R. Biochemistry 28, 3272–3280 (1989).
Blatt, M. R. J. Membrane. Biol. 102, 235–246 (1988).
Blatt, M. R. Planta 180, 445–455 (1990).
Blatt, M. R. Planta 170, 272–287 (1987).
Miller, A. J. & Sanders, D. Nature 326, 397–400 (1987).
Felle, H. Planta 174, 495–499 (1988).
Brosnan, J. M. & Sanders, D. FEBS Lett 260, 70–72 (1990).
Keller, B. U., Hedrich, R. & Raschke, K. Nature 341, 450–453 (1989).
MacRobbie, E. A. C. in Stomatal Function (eds Zeiger, E., Farquhar, G. D. & Cowan, I. R.) 125–162 (Stanford University Press, Stanford, California, 1987).
Blatt, M. R. J. Membrane Biol. 98, 257–274 (1987).
Blatt, M. R. & Slayman, C. L. J. Membrane Biol. 72, 223–234 (1983).
Walker, J., Reid, G. & Trentham, D. R. Meth. Enzym. 172, 288–301 (1989).
Fabiato, A. & Fabiato, F. J. Physiol., Paris 75, 463–505 (1979).
Pethie, R. et al. Cell Calcium 10, 491–497 (1989).
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Blatt, M., Thiel, G. & Trentham, D. Reversible inactivation of K+ channels of Vcia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate. Nature 346, 766–769 (1990). https://doi.org/10.1038/346766a0
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DOI: https://doi.org/10.1038/346766a0
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