... A de ned range of guard cell calcium oscillation parameters encodes stomatal movements
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1 535/4 nm rtio... A de ned rnge of gurd cell clcium oscilltion prmeters encodes stomtl movements Gethyn J. Allen*, Srh P. Chu*, Crrie L. Hrrington*, Krin Schumcher², Thoms Hoffmnn³, Yt Y. Tng*, Erwin Grill³ & Julin I. Schroeder* * Cell nd Developmentl Biology Section, Division of Biology nd Center for Moleculr Genetics, University of Cliforni, Sn Diego, L Joll, Cliforni , USA ² ZMBP-P nzenphysiologie, UniversitÈt TuÈingen, Auf der Morgenstelle 1, 776 TuÈingen, Germny ³ Technische UniversitÈt, MuÈnchen Lehrstuhl fur Botnik, D-8535 Freising±Weihenstephn, Germny... Oscilltions in cytosolic clcium concentrtion ([C 2+ ] cyt ) re centrl regultors of signl trnsduction cscdes 1, lthough the roles of individul [C 2+ ] cyt oscilltion prmeters in regulting downstrem physiologicl responses remin lrgely unknown. In plnts, gurd cells integrte environmentl nd endogenous signls to regulte the perture of stomtl pores 2 nd [C 2+ ] cyt oscilltions re fundmentl component of stomtl closure 3,4. Here we systemticlly vry [C 2+ ] cyt oscilltion prmeters in Aridopsis gurd cells using `clcium clmp' 3,5±7 nd show tht [C 2+ ] cyt controls stomtl closure y two mechnisms. Shortterm `clcium-rective' closure occurred rpidly when [C 2+ ] cyt ws elevted, wheres the degree of long-term stedy-stte closure ws `clcium progrmmed' y [C 2+ ] cyt oscilltions within de ned rnge of frequency, trnsient numer, durtion nd letters to nture mplitude. Furthermore, in gurd cells of the mutnt 8, [C 2+ ] cyt oscilltions induced y scisic cid nd extrcellulr clcium hd incresed frequencies nd reduced trnsient durtion, nd stedy-stte stomtl closure ws olished. Experimentlly imposing [C 2+ ] cyt oscilltions with prmeters tht elicited closure in the wild type restored long-term closure in stomt. These dt show tht de ned window of gurd cell [C 2+ ] cyt oscilltion prmeters progrms chnges in stedy-stte stomtl perture. In niml cells, [C 2+ ] cyt oscilltions cn regulte the ctivtion of downstrem components of signlling cscdes 5±7,9±12. In plnt cells, [C 2+ ] cyt oscilltions occur in response to mny stimuli 3,13±17, ut hypotheses tht oscilltion kinetics control physiologicl responses in plnts 4,18 hve not een systemticlly investigted. We incuted Aridopsis gurd cells expressing the green- uorescent-proteinsed clcium indictor yellow cmeleon 2.1 (see Methods) 19, for 2.5 h in the light in high KCl ( mm) uffer to elicit stomtl opening. These gurd cells showed stle, low resting [C 2+ ] cyt level, nd stomtl perture remined constnt for the susequent 3 h (see Supplementry Informtion Fig. 1). The in ux of extrcellulr clcium ([C 2+ ] ext ) into gurd cells is enhnced y plsm memrne hyperpolriztion 3,21±24. [C 2+ ] cyt oscilltions were imposed in gurd cells y repetedly chnging etween the high ( mm) KCl uffer (depolrizing uffer) nd low (.1 mm) KCl uffer contining 1 mm clcium (hyperpolrizing uffer) 3 (Fig. 1). Exchnges etween the depolrizing nd hyperpolrizing uffers every creted oscilltions in gurd cell [C 2+ ] cyt with xed 1-min hyperpolriztion to hyperpolriztion period (Fig. 1). Continuous repetitive exchnges induced 5±9 trnsients, depending on the degree of ttenution in individul gurd cells (six shown in Fig. 1, ottom pnel). Following the imposed oscilltions, gurd cells were returned to the depolrizing uffer under white light, nd the stedy-stte pertures were Trnsient Numer 35 Stedy-stte perture (% decrese) R Numer of trnsients Depolrizing uffer Hyperpolrizing uffer Figure 1 Incresing the numer of [C 2+ ] cyt trnsients decreses stedy-stte stomtl perture., Incresing numer of [C 2+ ] cyt trnsients imposed in gurd cells y repetitive exchnges etween depolrizing nd hyperpolrizing uffers., Stedy-stte stomtl perture following incresing numers of [C 2+ ] cyt trnsients. R denotes repetitive exchnges inducing 6±9 trnsients (s in ottom pnel of ). Stedy-stte perture chnges were clculted s percentge decrese nd re plotted s descending points to indicte stomtl closure. NATURE VOL JUNE Mcmilln Mgzines Ltd 153
2 535/4 nm rtio 535/4 nm rtio letters to nture mesured 3 h fter the strt of the oscilltion. An incresing numer of [C 2+ ] cyt trnsients elicited progressively lrger decreses in stedy-stte stomtl perture, with four or more trnsients cusing decrese of 55±% (Fig. 1). Enhnced stomtl closing induced y incresing the numer of [C 2+ ] cyt trnsients (Fig. 1, ) ws not due to gurd cells responding to greter overll [C 2+ ] cyt increse, ecuse three 5-min [C 2+ ] cyt trnsients elicited much greter stedy-stte stomtl closure thn 15-min [C 2+ ] cyt plteu 3 even though the totl [C 2+ ] cyt increse ws similr (P..56; see Supplementry Informtion Fig. 2; totl integrted [C 2+ ] cyt increse ws 3, nm min -1 for three 5-min trnsients (n = 22) nd 3, nm min -1 for 15-min plteu (n = 3)). Three imposed [C 2+ ] cyt trnsients hd similr mgnitudes (Fig. 1), showed little ttenution nd elicited ner-mximl stomtl closure ( %, Fig. 1), nd were therefore used s stndrd tretment to investigte whether other [C 2+ ] cyt oscilltion prmeters ffected stomtl perture. The effect of [C 2+ ] cyt oscilltion frequency on stedy-stte stomtl perture ws investigted y imposing oscilltions with ltencies of 2, 5, 1 or 1 etween three 5-min [C 2+ ] cyt trnsients. The resulting oscilltions hd periods of 7, 1, 15 or min (Fig. 2). An optiml [C 2+ ] cyt oscilltion period of 1 min ws pprent (Fig. 2) with reduced stomtl closure t longer or shorter periods. These dt indicte tht in gurd cells n optiml frequency of [C 2+ ] cyt oscilltion is required to elicit mximl reduction in stedy-stte stomtl perture. By vrying the low-kcl uffer perfusion time, the durtion of c Trnsient period Depolrizing uffer Trnsient durtion 7 min 1 min 1 Stedy-stte perture (% decrese) min Hyperpolrizing uffer d 2 min 8 min Stedy-stte perture (% decrese) Period (min) Durtion (min) Figure 2 The period nd durtion of [C 2+ ] cyt trnsients lters stedy-stte stomtl perture., Three 5-min [C 2+ ] cyt trnsients imposed in gurd cells with 7, 1, 15 or - min periods., Stedy-stte stomtl perture following imposed [C 2+ ] cyt oscilltions s in. c, Three [C 2+ ] cyt trnsients imposed in gurd cells with 2, 5 or 8-min durtion. Dshed lines indicte the xed period. d, Stomtl perture following imposed [C 2+ ] cyt oscilltions s in c. See lso Supplementry Informtion Fig Mcmilln Mgzines Ltd NATURE VOL JUNE 1
3 letters to nture [C 2+ ] cyt trnsients in gurd cells ws vried with constnt 1-min period. Three trnsients were imposed, ech with 1, 2, 5 or 8-min durtion (Fig. 2c). Trnsients with 5-min durtion elicited the gretest decrese in stedy-stte stomtl perture (Fig. 2d), wheres closure ws reduced with 2 or 8-min trnsients (Fig. 2d). A similr optimum for stomtl closure ws mesured if the trnsient durtion ws vried nd the high-kcl uffer perfusion time etween [C 2+ ] cyt trnsients ws kept constnt t (dt not shown). These dt indicte tht n optiml [C 2+ ] cyt trnsient durtion during [C 2+ ] cyt oscilltions is lso required to elicit mximl stomtl closure (Fig. 2d). A minimum trnsient durtion greter thn 1 min ws lso required to elicit signi cnt stedy-stte closure (Fig. 2d; see lso Supplementry Informtion Fig. 3). Reducing the mplitude of [C 2+ ] cyt oscilltions lso reduced stomtl closure (see Supplementry Informtion Fig. 4). To investigte short-term regultion of stomtl perture during the progression of [C 2+ ] cyt oscilltions, stomtl pertures were mesured 1 min fter ech [C 2+ ] cyt trnsient during imposed oscilltions with 1 or -min periods (Fig. 3). Oscilltions with these periods gve the gretest difference in stedy-stte perture chnge (Fig. 2). Stomtl perture decresed y round 45% immeditely fter n initil [C 2+ ] cyt trnsient nd decresed further following susequent trnsients y mximum of round 65%, irrespective of the oscilltion period (Fig. 3, ). When the oscilltion hd period of 1 min, stedy-stte stomtl pertures were still reduced y round 55% fter 3 h (Fig. 3). Following n oscilltion with -min period, however, stomt re-opened over the susequent 1±1.5 h to rech stedy-stte perture tht ws close to tht efore the oscilltion (Fig. 3). A -min [C 2+ ] cyt plteu tht filed to evoke stedy-stte chnge in perture 3 (Fig. 3c) lso induced short-term stomtl closure. Figure 3 shows tht [C 2+ ] cyt oscilltions cuse stomtl closure y two mechnisms. The rst is `clcium rective' nd cuses rpid, short-term closure when [C 2+ ] cyt is elevted. The second is long-term `clcium progrmmed' decrese in the stedy-stte perture, the degree of which is encoded y the frequency, trnsient numer, durtion nd mplitude of [C 2+ ] cyt oscilltions (Figs 1±3). Therefore, following clcium-rective closure, gurd cells cn elicit progrmmed chnges in perture y decoding the informtion contined in [C 2+ ] cyt oscilltion prmeters. The pproprite [C 2+ ] cyt oscilltion prmeters inhiited stomtl opening. We screened i1-1, i2-1 (ref. 25), er1-2 (ref. 26) nd (ref. 8) Aridopsis mutnts, ll of which exhiit errnt gurd cell scisic cid (ABA) signlling 8,25,27,28, to investigte whether these muttions ltered [C 2+ ] cyt oscilltion kinetics. We found tht [C 2+ ] ext -induced [C 2+ ] cyt oscilltion kinetics were mrkedly different from the wild type in gurd cells (Fig. 4). The recessive mutnt (growth controlled y scisic cid) is insensitive to ABA in its root growth nd stomtl response 8. Stomt of re lso impired in the closure response to H 2 O 2, nd ctivtion of plsm memrne clcium chnnel y H 2 O 2 is disrupted 24. In wild-type gurd cells, endogenous [C 2+ ] cyt oscilltions elicited y rising [C 2+ ] ext from 5 mm to 1 mm (with constnt 5-mM KCl uffer 3,14,17, ) hd period of min nd trnsient durtion of min (n = 46 cells), wheres in gurd cells 1 mm [C 2+ ] ext elicited oscilltions of similr mplitude (P..46) ut with much shorter period ( min, P,.1) nd trnsient durtion ( min, P,.1; n = 38 cells; Fig. 4). Stedy-stte stomtl closure in response to [C 2+ ] ext ws olished in (Fig. 4). The physiologicl stimulus ABA (5 mm) elicited [C 2+ ] cyt oscilltions with period of min nd trnsient durtion of min in wild-type gurd cells (n = 23 cells; Fig. 4c). In gurd cells, ABA-induced oscilltions hd signi cntly reduced period of (n =24,P,.3) nd trnsient durtion of min (P,.4; Fig. 4c). Stomtl closure in ws lso insensitive to ABA (Fig. 4d). To investigte whether C 2+ rective or progrmmed stomtl closure is disrupted in the mutnt, [C 2+ ] cyt oscilltions composed of three 5-min trnsients t 1-min periods were experimentlly imposed in gurd cells (n = 24, Fig. 5). Both clciumrective short-term closure nd clcium-progrmmed long-term closure were restored to round 75% of the wild-type level y these c 1 1-min period 1 -min period -min plteu 1 Figure 3 Preceding [C 2+ ] cyt oscilltion kinetics progrm stedy-stte stomtl perture., Stomtl perture chnges mesured during imposed [C 2+ ] cyt oscilltions with periods of 1 min., Stomtl perture chnges mesured during imposed [C 2+ ] cyt oscilltions with periods of min. c, Stomtl perture chnges mesured during -min imposed [C 2+ ] cyt plteu 3. Apertures were mesured for the lst min of the 2.5-h opening period (efore time t = ) nd for totl of 3 h fter t =. Cells were returned to the depolrizing uffer following the imposition of [C 2+ ] cyt increses. Note scle chnges on x-xis re for perture mesurements only. RU = 535/4-nm rtio units. Dt re the men 6 s.e.m. reltive to n = 4 replictes comprising 12 individully mpped stomtes. NATURE VOL JUNE Mcmilln Mgzines Ltd 155
4 535/4 nm rtio 535/4 nm rtio letters to nture endogenous mm C endogenous mm C 2+ c 1.1 endogenous ABA 1 min 1. endogenous ABA Stedy-stte stomtl perture (% decrese) d Stedy-stte stomtl perture (% decrese) [C 2+ ] ext (mm) [ABA] (µm) Figure 4 Altered [C 2+ ] cyt oscilltion kinetics nd stomtl closure in the mutnt., [C 2+ ] cyt oscilltions elicited y 1 mm [C 2+ ] ext in wild-type (top) nd (ottom) gurd cells., Stedy-stte stomtl perture chnges elicited y [C 2+ ] ext in wild-type (closed symols) nd (open symols). c, [C 2+ ] cyt oscilltions elicited y 5 mm ABA in wild-type (top) nd (ottom) gurd cells. d, Stedy-stte stomtl perture chnges elicited y ABA in wild-type (closed symols) nd (open symols). Dt in nd d re men 6 s.e.m. reltive to n = 3 replictes comprising stomtes per point min durtion 4.5-min period Figure 5 Altered [C 2+ ] cyt oscilltion kinetics in prevent long-term stomtl closure., Stomtl perture chnges mesured during imposed [C 2+ ] cyt oscilltions with periods of 1 min in gurd cells., Stomtl perture chnges mesured in wild type nd during imposed [C 2+ ] cyt oscilltions tht mimic stimulus-induced oscilltions in gurd cells. Note imposed oscilltions hd n mplitude,3% greter thn endogenous oscilltions, which my enhnce short-term responses. Cells were returned to the depolrizing uffer fter the imposition of the oscilltion. Scle chnges on x-xis re for perture mesurements only. RU = 535/4-nm rtio units. Dt re the men 6 s.e.m. reltive to n = 3 replictes comprising nine individully mpped stomtes per trce Mcmilln Mgzines Ltd NATURE VOL JUNE 1
5 letters to nture imposed oscilltions (Fig. 5, compre to Fig. 3). The 75% response indictes tht my hve prtil effects on dditionl mechnisms downstrem of [C 2+ ] cyt increses. Additionlly, to mimic stimulus-induced [C 2+ ] cyt oscilltions in gurd cells, oscilltions composed of four [C 2+ ] cyt trnsients of 1.7 durtion t 4.5-min periods were imposed in oth wild-type nd gurd cells (Fig. 5). These prmeters represent the men durtion nd frequency of [C 2+ ] ext - nd ABA-induced oscilltions in gurd cells (Fig. 4, c). These oscilltions elicited clciumrective stomtl closure in oth wild-type nd cells, ut filed to elicit ny long-term chnge in perture through the clciumprogrmmed response (Fig. 5). Overll, Fig. 5 shows tht gurd cells remin competent to respond to [C 2+ ] cyt oscilltions if the trnsient durtion nd frequency re within the rnge required to elicit long-term stedy-stte stomtl closure (Fig. 5). Furthermore, stimulus-induced [C 2+ ] cyt oscilltions in gurd cells, lthough suf cient to cuse clcium-rective closure, hve kinetics outside the `window' necessry to elicit clcium-progrmmed chnge in stedy-stte perture. The [C 2+ ] cyt oscilltions imposed in this study re similr to previously reported gurd cell [C 2+ ] cyt oscilltions induced y physiologicl stimuli: trnsients re symmetric (the rise in [C 2+ ] cyt eing fster thn the decy) nd successive trnsients show ttenution 3,14,17,23,24,29,3. ABA, oxidtive stress nd [C 2+ ] ext induce [C 2+ ] cyt oscilltions in gurd cells with periods etween 6 nd 12 min nd induce 25±5% stomtl closure 3,14,17,24,3, which is consistent with the degree of stomtl closure induced y similr imposed oscilltions in this study. Recently, [C 2+ ] ext ws shown to elicit [C 2+ ] cyt plteux in gurd cells of the Aridopsis V-ATPse mutnt det3 nd stedy-stte stomtl closure ws olished 3. However, the det3 response gives no indiction of whether individul [C 2+ ] cyt oscilltion prmeters ffect stomtl closure. The ltertion of the frequency nd trnsient durtion of [C 2+ ] cyt oscilltions in gurd cells nd the disruption of stedy-stte stomtl closure (Figs 4, 5) clerly show tht the cpcity to generte pproprite gurd cell [C 2+ ] cyt oscilltions is ffected in. This ltertion of stimulus-induced [C 2+ ] cyt oscilltion kinetics is the predominnt fctor in preventing long-term clcium-progrmmed chnge in stomtl perture. To our knowledge, disruption of clcium-progrmmed stomtl closure in nd the ltertion of periodic defection pttern in the dec-4 Cenorhditis elegns mutnt 12 re the only exmples for which modultion of physiologicl response hs een directly correlted to chnge in [C 2+ ] cyt oscilltion kinetics. Overll, these dt provide physiologicl nd genetic evidence tht the kinetics of [C 2+ ] cyt oscilltions in gurd cells cn control stedy-stte stomtl perture chnges 4,18 nd therefore show tht [C 2+ ] cyt oscilltion kinetics in plnt cells cn encode informtion tht controls the mgnitude of grded physiologicl response. M Methods Plnt growth A. thlin ws grown with 16-h light/8-h drk cycle nd photon uency rte of 75 mmol m -2 s -1 t 8C. Clcium imging We performed clcium imging nd clirtion s descried 3,. We incuted xil epiderml strips for 2.5 h in the light (125 mmol m -2 s -1 ) in mm KCl, CCl 2 nd 1 mm Mes-Tris ph 6.15 (depolrizing uffer) to open stomt. [C 2+ ] cyt trnsients were imposed y rpid (1 s) exchnge of the chmer uffer etween this depolrizing uffer nd.1 mm KCl, 1 mm CCl 2 nd 1 mm Mes-Tris ph 6.15 (hyperpolrizing uffer). We mesured imposed oscilltions in 16±38 cells for ech tretment; they were highly reproducile etween cells. Bseline decreses in emission rtios due to leching were sutrcted. The 535/4-nm rtios re smller thn previously reported 3,,24 ecuse we used CCD cmer with improved 4-nm sensitivity. We mesured endogenous oscilltions (Fig. 4) in 5 mm KCl, 5 mm CCl 2 nd 1 mm Mes-Tris ph 5.6. In these conditions, 32% of gurd cells exhiited spontneous oscilltions, which were similr in wild-type nd (P..5). Only cells exhiiting stle resting [C 2+ ] cyt were used to nlyse stimulus-induced oscilltions. ABA-induced [C 2+ ] cyt increses were oserved in 72% of cells (47 of 65 cells). Stomtl perture mesurements Stomt were opened nd oscilltions imposed using the sme method s for imging. After imposition of n oscilltion, cells were mintined in the ( mm KCl) depolrizing uffer nd stedy-stte chnges in perture rtio (width/length) were mesured s descried 3 efore nd 3 h fter the initition of [C 2+ ] cyt oscilltions (Figs 1, 2 nd 4) or throughout the oscilltion (Figs 3 & 5). Apertures re men 6 s.e.m. reltive to n = 4 replictes comprising 1 stomtes, unless otherwise stted. Received 27 Octoer ; ccepted 27 April Berridge, M. J. The AM nd FM of clcium signlling. Nture 386, 759±7 (1997). 2. McRoie, E. A. C. Signlling in gurd cells nd regultion of ion chnnel ctivity. J. Exp. Bot. 48, 515±528 (1997). 3. Allen, G. J. et l. Altertion of stimulus-speci c gurd cell clcium oscilltions nd stomtl closing in Aridopsis det3 mutnt. Science 289, 2338±2342 (). 4. McAinsh, M. R. & Hetherington, A. M. Encoding speci city in C 2+ signlling systems. Trends Plnt Sci. 3, 32±36 (1998). 5. Gu, X. & Spitzer, N. C. Distinct spects of neuronl differentition encoded y frequency of spontneous C 2+ trnsients. Nture 375, 784±787 (1995). 6. Dolmetsch, R. E., Xu, K. & Lewis, R. S. Clcium oscilltions increse the ef ciency nd speci city of gene expression. Nture 392, 933±936 (1998). 7. De Koninck, P. & Schulmn, H. Sensitivity of CM kinse II to the frequency of C 2+ oscilltions. Science 279, 227±23 (1998). 8. Himmelch, A., Iten, M. & Grill, E. Signlling of scisic cid to regulte plnt growth. Phil. Trns. R. Soc. Lond. B 353, 1439±1444 (1998). 9. Li, W. et l. Cell-perment cge InsP 3 ester shows tht C 2+ spike frequency cn optimize gene expression. Nture 392, 936±941 (1998). 1. Gomez, T. M & Spitzer, N. C. In vivo regultion of xon extension nd pth nding y growth-cone clcium trnsients. Nture 397, 35±355 (1999). 11. Cmcho P, & Lechleiter, J. D. Incresed frequency of clcium wves in Xenopus levis oocytes tht express clcium-atpse. Science 2, 226±229 (1993). 12. Dl Snto, P., Logn, M. A., Chisholm, A. D. & Jorgensen, E. M. The inositol trisphosphte receptor regultes 5-second ehviorl rhythm in C. elegns. Cell 98, 757±767 (1999). 13. Felle, H. Auxin cuses oscilltions of cytosolic free clcium nd ph in Ze mys coleoptiles. Plnt 174, 495±499 (1988). 14. McAinsh, M. R., We, A. A. R., Tylor, J. E. & Hetherington, A. M. Stimulus-induced oscilltions in gurd cell cytoplsmic free clcium. Plnt Cell 7, 7±1219 (1995). 15. Ehrhrdt, D. W., Wis, R. & Long, S. R. Clcium spiking in plnt root hirs responding to rhizoium nodultion signls. Cell 85, 673±681 (1996). 16. Holdwy-Clrke, T. L., FeijoÂ, J. A.,Hckett, G. R., Kunkel,J. G. &Hepler, P. K. Pollen tue growth nd intrcellulr cytosolic clcium grdient oscillte in phse while extrcellulr clcium in ux is delyed. Plnt Cell 9, 1999±1 (1997). 17. StxeÂn, I. et l. Ascisic cid induces oscilltions in gurd-cell cytosolic free clcium tht involve phosphoinositide-speci c phospholipse C. Proc. Ntl Acd. Sci. USA 96,1779±1784 (1999). 18. Trewvs, A. J. & Mlho, R. C 2+ signlling in plnt cells: the ig network! Curr. Opin. Plnt Biol. 1, 428±433 (1998). 19. Miywki, A., Grieseck, O., Heim, R. & Tsien, R. Y. Dynmic nd quntittive C 2+ mesurements using improved cmeleons. Proc. Ntl Acd. Sci. USA 96, 2135±21 (1999).. Allen, G. J. et l. Cmeleon clcium indictor reports cytoplsmic clcium dynmics in Aridopsis gurd cells. Plnt J. 19, 735±747 (1999). 21. Gilroy, S., Fricker, M. D., Red, N. D. & Trewvs, A. J. Role of clcium in signl trnsduction of commelin gurd-cells. Plnt Cell 3, 333±344 (1991). 22. Grov, A. & Bltt, M. R. Memrne voltge initites C 2+ wves nd potentites C 2+ increses with scisic cid in stomtl gurd cells. Proc. Ntl Acd. Sci. USA 95, 4778±4783 (1998). 23. Hmilton, D. W., Hills, A., Kohler, B. & Bltt, M. R. C 2+ chnnels t the plsm memrne of stomtl gurd cells re ctivted y hyperpolriztion nd scisic cid. Proc. Ntl Acd. Sci. USA 97, 4967± 4972 (). 24. Pei, Z. M. et l. Hydrogen peroxide-ctivted C 2+ chnnels medite gurd cell scisic cid signlling. Nture 6, 731±734 (). 25. Koornneef, M., Reuling, G. & Krssen, C. M. The isoltion nd chrcteristion of scisic cidinsensitive mutnts of Aridopsis thlin. Physiol. Plnt 61, 377±383 (1984). 26. Cutler, S., Ghssemin, M., Bonett, D., Cooney, S. & McCourt, P. A protein frnesyl trnsferse involved in scisic cid signl trnsduction in Aridopsis. Science 273, 1239±1241 (1996). 27. Pei, Z. M., Ghssemin, M., Kwk, C. M., McCourt, P. & Schroeder, J. I. Role of frnesyltrnsferse in ABA regultion of gurd cell nion chnnels nd plnt wter loss. Science 282, 287±29 (1998). 28. Pei, Z. M. et l. Differentil scisic cid regultion of gurd cell slow nion chnnels in Aridopsis wild-type nd i1 nd i2 mutnts. Plnt Cell 9, 9±423 (1997). 29. Schroeder, J. I. & Hgiwr, S. Repetitive increses in cytoplsmic C 2+ of gurd cells y scisic cid ctivtion of non-selective C 2+ -permele chnnels. Proc. Ntl Acd. Sci. USA 87, 935±939 (199). 3. Bltt, M. R. C 2+ signlling nd control of gurd-cell volume in stomtl movements. Curr. Opin. Plnt Biol. 3, 196±4 (). Supplementry Informtion is ville on Nture's World-Wide We site ( or s pper copy from the London editoril of ce of Nture. Acknowledgements We thnk J. Hrper for discussions nd N. Spitzer nd R. Tsien for comments on the mnuscript. This reserch ws supported y NIH, Deprtment of Energy nd Ntionl Science Foundtion grnts to J.I.S. nd DFG grnt nd Fonds der Chemischen Industrie to E.G. Correspondence nd requests for mterils should e ddressed to J.I.S. (e-mil: Julin@iomil.ucsd.edu). NATURE VOL JUNE Mcmilln Mgzines Ltd
SUPPLEMENTARY INFORMATION
doi:1.138/nture1794 BR EPFs BRI1? ERECTA TMM BSKs YDA PP2A BSU1 BIN2 pbzr1/2 BZR1/2 MKK4/5/7/9 MPK3/6 SPCH Cell growth Stomtl production Supplementry Figure 1. The model of BR nd stomtl signling pthwys.
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