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PNAS 100 (17): 10091-10095

Copyright © 2003 by the National Academy of Sciences.

BIOLOGICAL SCIENCES / PLANT BIOLOGY

Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells

Fouad Lemtiri-Chlieh*,{dagger}, Enid A. C. MacRobbie*, Alex A. R. Webb*, Nick F. Manison{ddagger}, Colin Brownlee{ddagger}, Jeremy N. Skepper§, Jian Chen, Glenn D. Prestwich, and Charles A. Brearley||,**

*Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom; {ddagger}Marine Biological Association, Citadel Hill, Plymouth PL1 2PB, United Kingdom; §Multi-Imaging Centre, Department of Anatomy, University of Cambridge, Tennis Court Road, Cambridge CB2 3DY, United Kingdom; Department of Medicinal Chemistry, University of Utah, 419 Wakara Way, Suite 205, Salt Lake City, UT 84108; and ||School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom

Contributed by Enid A. C. MacRobbie, May 30, 2003

Abstract: myo-Inositol hexakisphosphate (InsP6) is the most abundant inositol phosphate in cells, yet it remains the most enigmatic of this class of signaling molecule. InsP6 plays a role in the processes by which the drought stress hormone abscisic acid (ABA) induces stomatal closure, conserving water and ensuring plant survival. Previous work has shown that InsP6 levels in guard cells are elevated in response to ABA, and InsP6 inactivates the plasma membrane inward K+ conductance (IK,in) in a cytosolic calcium-dependent manner. The use of laser-scanning confocal microscopy in dye-loaded patch-clamped guard cell protoplasts shows that release of InsP6 from a caged precursor mobilizes calcium. Measurement of calcium (barium) currents ICa in patch-clamped protoplasts in whole cell mode shows that InsP6 has no effect on the calcium-permeable channels in the plasma membrane activated by ABA. The InsP6-mediated inhibition of IK,in can also be observed in the absence of external calcium. Thus the InsP6-induced increase in cytoplasmic calcium does not result from calcium influx but must arise from InsP6-triggered release of calcium from endomembrane stores. Measurements of vacuolar currents in patch-clamped isolated vacuoles in whole-vacuole mode showed that InsP6 activates both the fast and slow conductances of the guard cell vacuole. These data define InsP6 as an endomembrane-acting calcium-release signal in guard cells; the vacuole may contribute to InsP6-triggered Ca2+ release, but other endomembranes may also be involved.

** To whom correspondence should be addressed. E-mail: c.brearley{at}uea.ac.uk.

{dagger} Present address: Department of Plant Science, 4-4067, University of Connecticut, 1376 Storrs Road, Storrs, CT 06269.

Abbreviations: ABA, abscisic acid; IK,in,K+-inward rectifier; InsP6, myo-inositol hexakisphosphate; FV, fast vacuolar; SV, slow vacuolar; GCP, guard cell protoplast; cADPR, cyclic adenosine diphosphoribose; Ins(1,4,5)P3, inositol 1,4,5-trisphosphate; I–V, current–voltage.

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