Cousson Et Al., 1998 Two Potential...

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Plmr Physiol. B iochcm, 1998, 36 (3). 257-262

Two potential Ca2+ dependent transduction pathways in stomata1closing in response to abscisic acidAlain Cowson*, Alain VavasseurLaboratoiredeBioCnergCtique Cellulaire, CEA/Cadarache-DSV DEVM, (CNRS-CEA, UMR 163).13 108 Saint-Paul-lez-Durance cedex, France.* Author to whom correspondence should be addressed (fax 33 (0) 42 25 46 56; e-mail [email protected])

(Received April 21, 1997; accepted June 7, 1997)

Abstract - Withering of abscisic acid (ABA)-insensitive mutants in standard watering conditions as well as under droughtsuggests that ABA would regulate stomata1 closing not only under water stress but also under other hydric conditions. Depen-ding on its applied concentration, the ABA closing signal might be transduced through different pathways. This possibility wasinvestigated in epidermal peels of Commelina communis by comparing the effects of different Ca + buffers, protein kinase inhi-bitors, calmodulin (CaM) antagonists and guanosine-triphosphate-binding protein (G protein) modulators on the stomata1closing responses to 10 nM ABA (ABA,,,) and 100 nM ABA (ABA,,,,). EGTA speci fica lly suppressed the response to ABA,, ,,while the Ca*+ buffer 1,2-bis(o-aminophenoxy)ethane-N,N,N X-tetraacetic acid (BAPTA) similarly inhibited the responses toABA,,, and ABA,,,,. The response to ABA,, was specif ically affec ted by the protein kinase inhibitors KT5926 and I-(5.iodo-naphthalene- 1 sulphonyl)- 1H-hexahydro- 1,4-diazepine (ML-7), the CaM antagonist N-(6.aminohexyl)-5-chloro- 1 naphthalene-sulfonamide (W-7), and the phospholipase C inhibitor 1-[6-[[ 17B-3-methoxyestra-1,3,5(10)-trien- 17-yl]amino]hexyl]-1 H-pyrrole-2,5-dione (LJ73122), whereas the response to ABA,tx, was speci fically affec ted by the G protein antagonist pGlu-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH? (GP Ant-2) and mas17, an inactive mastoparan analog. These data are consistent with twopossible ABA routes, each of them exhibiting specifi c Cal+-requirements and protein phosphorylations. and being initiated byits own receptor. Furthermore, analogies with animal features suggest that the ABA,,, and ABA,,,,, closing signals might be extra-cellularly perceived. 0 Elsevier, Paris.Abscisic acid I Ca+ buffers I guanosine-triphosphate-binding protein modulators / protein phosphorylation / receptors /stomata1 closing I Commelina communisABA,,, 10 nM ABA/ ABA,, 1, 100 nM ABA / BAPTA, 1,2-bis(o-aminophenoxy)ethane-N,N,N,N-tetraacetic acid I CaM,calmodulin / Ca+-CaM, Ca +-calmodulin complex / DAG, l&diacylglycerol / GP Ant-2, pGlu-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH, / GP Ant-ZA, Arg-Pro-Lys-Pro-Gln-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH~ / H-7, 1-(5iso-quinolinesul-phonyl)-2-methylpiperazine / InsP3, inositol 1,4,5triphosphate / ML-7, I-(5iodonaphthalene-l-sulphonyl)-lH-hexa-hydro-1,4-diazepine / MLCK, myosin light chain kinase / U73122, 1-[6-[[17~-3-methoxyestra-1,3,5(10)-trien-17-yl]ami-no]hexyl]-lH-pyrrole-2,5-dione / U73343, 1-[6-[[17~-3-methoxyestra-1,3,5(lO)-trien-l7-yi]amino]hexyl]-2~-pyrrolidine-dione / W-5, N-(6-aminohexyl)-1-naphthalenesulphonamide/ W-7, N-(6-aminohexyl)-5-chloro-l-naphthalenesulphona-mide / 7TMS, 7 trans-membrane span

1. INTRODUCTIONPlants respond to water stressby reducing transpi-ration through abscisic acid (ABA) which induces

closing of the stomata1pores in the leaves [4]. It isknown that micromolar concentrations of externalABA induce the stomata to close through increases ncytosolic free Ca+ [14] and protein phosphorylation[ 181.Moreover, recent studies [2] suggest hat, withinthe ABA signal transduction, G protein-linked seven-transmembrane-span (7TMS) receptors regulateplasmamembraneK+ channelsof stomata1 uard cells.

Withering of ABA-insensitive mutants [lo] in stan-dard hydric conditions suggests hat endogenousABAwould regulate stomata1 closing under conditionsother than water stress.Also, it is important to ques-tion whether or not endogenousABA would respondto different watering conditions by the same regula-tory mechanisms of stomata1closing. In the leaves.the concentration of endogenous ABA might dependon the applied watering conditions. In this context,one can suppose that, according to its concentration,endogenous ABA might modulate stomata1 closingvia different possible transduction pathways.

Plant Physiol. Biochem ., 0981-9428/98/03/O Elsevier, Paris


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258 A. Cousson, A. Vavasseur

This hypothesis hasbeen investigated by examiningwhether different concentrations of exogenouslyapplied ABA trigger different signal transductionpathways leading to stomata] closing in epidermalpeels of Commelina communis. For such a purpose,two concentrations of exogenously applied ABA havebeen retained, e.g. 10 nM ABA (ABA,,,) which signi-ficantly limits stomata1 closure and 100 nM ABA .(ABA,,,) which induces almost maximum stomata1closure [ 141. ndeed, these ABA concentrations wouldmimic the ABA status encountered in the leavesduring either standard watering or water stress. In acomparative study of the stomata1 losing responses oABA,, and ABA,,, various compounds have beenassayed such as different Ca+ buffers, calmodulin(CaM) antagonists and selective inhibitors whichblock protein phosphorylations or prevent differentclassesof heterotrimeric guanosine-triphosphate-bind-ing regulatory proteins (G proteins) from functioning.

2. RESULTS AND DISCUSSION2 1 Effect of Ca2+ buffers.

In agreement with McAinsh et al. [14], ABA,,, andABA,, induced the meanstomata1 perture to decreaseby 6.5 and 11.0 urn respectively (figure f ). Figure Ishows that Ca*+-dependencyof the response o ABA,,,differs from that exhibited by the response o ABA,,,,.Indeed, the Ca2+ buffer EGTA largely inhibited sto-matal closing to ABA,Y but not to ABA,,, cfigure I A).By contrast, the Ca-+ buffer 1,2-bis(o-aminophe-noxy)ethane-N,N, N *,N -tetraacetic acid (BAPTA)almost completely suppressed stomata] closing toABA,, as well as to ABAr,, @gure I B). SinceBAPTA, but not EGTA, could buffer efficiently rapidincreases n cytosolic free Cal+ [2], our data suggestthat, among the possible Ca2+ transients, rapid onescould be predominantly involved in the response toABA,. These transients might mediate particularsteps within the ABA transduction pathway, includingprotein phosphorylation. The possibility that theresponses o ABA,,, and ABA,,, might be discrimi-nated by Ca2+-dependent hosphorylations was nvesti-gated by using protein kinase inhibitors and CaMantagonistswhich selectively prevent different types ofCa+-dependent processes.2.2. Effect of protein kinase inhibitors and CaMantagonists

The protein kinase inhibitors I-(5-isoquinolinesul-phonyl)-2-methylpiperazine (H-7), K-252a, KT.5926

0 1 2 0 1 2EGTA conch (mM) BAPTA cont. (mM)

Figure 1. Modulation of ABA-induced stomata1 closing by Ca+ buf-fers. Differential inhibitory effect of the Ca buffers (A) EGTA and(B) BAP TA on the induction of stomata1 closing by IO nM ABA (0)or 100 nM AB A (0). Extent in stomata1 closing is taken as the difter-ewe between the stomata1 apertures measured just before and 2 h afterthe addition of ABA. Each data point represents the mean -t SE cal-culated from 4 independent experiments.

and I-(5-iodonaphthalene-l-sulphonyl)-lH-hexahy-dro- 1,4-diazepine (ML-7) were tested: ML-7 selec-tively inhibits myosin light chain kinase (MLCK) [ 171which is also half inhibited by 97 PM H-7, 17 nM K-252a and 18 nM KT5926. Stomata1closing to ABA,,,was specifically suppressedby 1 yM KT5926 and20 @I ML-7, whereas 1 @I K-252a inhibited theresponses o both ABA,, and ABA,,,, (figure 2). Giventhe inhibitory properties to MLCK exhibited by ML-7and KT5926, our data suggest hat protein phosphory-lations catalysed by kinases of the MLCK type couldmediate the response o ABA,,. This is further sup-ported by the finding that, at the concentration of20 @I which is not inhibitory to MLCK, H-7 did notaffect the response o ABA ,() (figure 2 A).Although K-252a and KT5926 similarly inhibitMLCK, they differentially affected stomata1closing toABA,,,,, cfigure 2 B). Therefore, contrasting with theresponse o ABA,,, stomata] closing to ABA ,o0mightnot involve any kinases of the MLCK type. SinceMLCK activity depends on the Ca-CaM complex(Ca2+-CaM) [21], our data suggest that Ca2+-CaM

dependent protein phosphorylations or protein kinasesregulated by a CaM-like domain [16] might beinvolved in the response o ABA,, but not to ABA,,,,,.This was investigated by studying the effect of theCaM antagonists N-(6-aminohexyl)-l -naphthalenesul-phonamide (W-5) and N-(6aminohexyl)-5-chloro-l-naphthalenesulphonamide W-7) on the stomata] res-ponses o ABA,, and ABA,,,,,.Plant Physiol. B&hem .


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Ca*+-dependent stomata1 closing responses to abscisic acid 259

Figure 2. Influence of protein kinaae inhibitors on ABA-induced sto-matal closing. Differential eflect of the protein kinase inhibitors H-7(20 @I). K-252a (I pM), KT.5 926 (I ~.IM) and ML-7 (20 FM) on theinduction of stomata1 clos ing by (A) 10 nM ABA (ABA,,,) and (B)lOOnM ABA (ABA,,,,). Stomata] apertures were measured justbefore (base line) and 2 h after (columns) the application of ABA.Each experiment was at least duplicated.

The CaM antagonist W-7 (20 @VI) almostcompletely inhibited stomata1 closing to ABA,,(figure 3 A) but did not affect the response o ABA,,,,,(figure 3 B), whereas 20 pill W-5 did not significantlychange any of the two stomata1 esponses &uue 3 Aand B). The differential effect of W-5 and W-7 onABA,,,-induced stomat.al closing would be explainedby the less inhibitory action of W-5 on Ca+-CaMcompared to W-7 [9]. Therefore, these data are consis-tent with a possible implication of Ca-CaM depen-dent processes n the stomata1 esponse o ABA,,,. Incontrast, the fact that 20 pM W-7 did not inhibit sto-matal closing to ABA,,,,, suggest hat this last responsewould not involve any Ca+-CaM dependent process.This viewpoint is supported further by the fact thatother CaM antagonists, such as trifluoperazine andfluphenazine gave similar results to those obtainedwith W-7 (data not shown).

From all these data emerges he possibility that eachof the two ABA closing signals could be transducedthrough specific protein phosphorylations. In anattempt to characterize the ABA,,, and ABAloo closingsignals. the concentration of the protonated form ofABA, ABA(H), was modified by varying the externalpH at a constant concentration of exogenously appliedABA. Figure 4 shows that acidification of the bathingsolution induced a loss of sensitivity to ML-7 and W-7for the stomata1 closing responses to ABA,,, and

Figure 3. Influence of calmod ulin antagonists on ABA-induced sto-matal closing . Differential effect of the calmod ulin antagonists W-S(20 ~.IM) and W-7 (20 FM) on the induction of stomata1 closin g by (A)IO nM ABA (ABA,,) and (B) 100 nM ABA (ABA,,,). Stomata1 aper-tures were measured just before (base line) and 2 h after (columns) theapplication of ABA. Each experiment wab at lcast duplicated.

ABAloo. This change in sensitivity was observed at ahigher pH for the response to ABA,, (figure 4 Cand D) compared to the response o ABA,,, (figure 4 Aand B), which suggests hat the responses o ABA,,,and ABA,,,, would be determined by the ABA(H) con-centration. It is not possible from these results to con-clude whether the protonation is required for ABAuptake or for interacting with a receptor.2.3. Effect of inhibitors of G protein functioning

As suggested by figure I, the stomata1 closingresponses o ABA,,, and ABA,, would differentiallydepend on Ca2+, which might reflect differences intheir Ca7+ mobilization. To investigate whether par-ticular steps in Ca2+ mobilization would characterizethe type of ABA response, we searched or a possibledifferential effect of the aminosteroid 1-[6-[ [ 17p-3-methoxyestra-I ,3,5( lO)-trien-l7-yl]amino]hexyl]-lH-pyrrole-2,5-dione (U73 122) on the ABA,,, and ABA,,,,responses. ndeed, U73 122 is a selective inhibitor ofreceptor- coupled phospholipase C-dependent pro-cesses n mammalian cells, such as the production ofinositol I ,4.5-triphosphate (InsP,) and I ,2-diacylgly-cerol (DAG) and Cal+ mobilization [ 191.The aminosteroid U73122 (3 nM) half inhibited theresponse to ABA,, @gure 5B), whereas it did notaffect stomata1 losing to ABA,(,,, @gur-e5 C) even atconcentrations increasing up to the micromolar range.

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Figure 4. ABA-induced stomata1 clos ing as changed by the externalpH. Influence of the external pH on the modulation of ABA- inducedstoma ta1 clos ing by ML-7 (20 FM) and W-7 (20 yM). S toma ta1 aper-tures were measured just before (base line) and 2 h after (columns) theaddition of 10 nM ABA (ABA,,,) at (A) pH 6 or (B) pH 5, and of 100nM ABA (ABA,,,) at (C) pH 7 or (D) pH 6. Each experiment was atleast duplicated.

Moreover. in the absence of external ABA, U73122did not modify the mean stomata1 aperture(figure 5 A). Therefore, since InsP, [6] and DAG [ 111respectively induce stomata1 losing and opening, ourfinding could be explained by supposing that, withinthe ABA,, transduction pathway, U73122 couldinhibit phospholipaseC activity, resulting in the con-comitant decreases n InsP, and DAG concentrations:the drop in cellular DAG level would close partiallythe stomata1 ore, thereby preventing full inhibition ofstomata1 closing by U73 122. Since InsP, mobilizesCa2+ eserves n vivo [6] and releasesCa*+ from vacu-oles in vitro [I], our data suggest hat putative inhibi-tion of phosf holipase C by U73122 might block atleast one Ca mobilizing step specific to the ABA,,,response. Hypothesis that U73122 could inhibit phos-pholipase C in C. communis guard cells is supportedby the finding that the aminosteroid I-[6-[[ 17p-3-methoxyestra- 1,3,5( 10)-trien- 17-yl]amino]hexyl l-2,5-pyrrolidine-dione (U73343), a close analogue ofU73 122 which does not affect the activity of phospho-lipase C in mammalian cells [19], did not inhibit theresponse to ABA,,, at concentrations ranging fromnanomolar to micromolar values (figure 5 B, data notshown).

Within the surface receptor- G protein- phospholi-pase C transduction unit of mammalian cells, theaction site of U73122 could be at the level of G, pro-teins coupled to phospholipase CD 120, 22, 231 andlinked to specific 7TMS receptors [3]. These features,

0 L

Figure 5. Influence of inhibitors of G protein functioning on ABA-induced stomata1 closing. Differential effect of the G protein m odula-tors U73122 (3 nM), U73343 (3 nM), GP Ant-2A (10 FM), GP Ant-2(10 FM) and masl7 (5 FM) on (A) the maintenance of stomata1 open-ing in the light under COz-free air (-CO? + Light) and on the inductionof stomata1 clos ing by (B) 10 nM ABA (ABA,,) or(C) 100 nM ABA(ABA,,,,). Stomata1 aperture is measured jus t before (base line) and2 h after (columns) the addition of ABA. Each experiment was repli-cated at least 4 times.

together with the presenceof G protein-linked 7TMSreceptors in the plasma membrane of stomata1guardcells [2], suggest hat the ABA,, signal might be extra-cellularly perceived by a 7TMS-like receptor and spe-cifically transduced through G, protein mediatedactivation of phospholipaseCp. Reinforcing this hypo-thetical scheme is the inhibition of the response toABA,, by the G protein antagonist Arg-Pro-Lys-Pro-Gln-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH? (GP Ant2A) C&w-e 5 B) which selectively prevents activationof G, proteins in a competitive manner with 7TMSreceptors for G, protein binding [15]. However, byitself @gut-e 5 A) or in the presence of 100 nM ABA(figure 5 C), GP Ant-2A increased the mean stomata1aperture, indicating that inhibition of the response toABA,,, by GP Ant-2A might also result from a sideeffect.

Furthermore, the response o ABA,,, was specifi-cally affected by the inactive mastoparan analogmas17 and the G protein antagonist pGlu-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH2 (GP Ant-2) @gure 5). Inanimal systems, these compounds selectively inhibitactivation of G proteins other than G, proteins, such asGi proteins [7, 151 which have also been identified inplant systems [ 131. n animal cells, the G, and Gi pro-teins are linked to different types of receptor [7, 15, 31.


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Ca+-dependent stomata1 closing responses to abscisic acid 261

Therefore, taken together, our data support that each ofthe two Ca+-dependent stomata1 closing responses toABA might be initiated by its own receptor. Further-more, they do not exclude the possible involvement ofInsP, in the Ca2+ mobilizing step of the ABA,, trans-duction pathway, as recently suggested [121. Up tonow, only phosphoinositide-specific phospholipase Cisozymes closely related to the 6 subfamily have beenshown to be induced in plants by high ABA levels [S].Since regulation of phospholipase C6 in mammalianswould occur through reversible binding to the plasmamembrane [5], activity of these plant phospholipase Cisozymes might be stimulated by putative surfacereceptors via the functioning of as yet to be identifiedG proteins. In this context, one can propose that theABA,00 signal would be specifically transducedthrough a putative transmembrane unit composed of asurface receptor, a Gi protein and a phospholipase C6related isozyme.

3. CONCLUSIONOur data are consistent with the hypothesis that,depending on the concentration of its protonated formABA(H) in the apoplast, ABA might modulate sto-matal closing through one of two potential transduc-tion pathways that would differ in their Ca+dependencies and protein phosphorylation events. Fur-thermore, they suggest that each of these two putative

ABA routes might be initiated by its own receptor. Theconcentration of endogenous ABA(H) might vary inresponse to different watering conditions. Thus,according to water ava.ilability, ABA might regulateguard cell turgor via two possible Ca2+-dependenttransduction pathways. This scheme can contribute toour understanding of the molecular functioning ofABA in the guard cell and, more generally, to our con-cepts that the plant may respond differently to a givenhormone in a concentration-dependent manner.

4. METHODS4.1. Plant material. Commelina communis (L.) seeds weregerminated on moistened cellulose tissue for 10 d. The seed-lings were then transferred to pots of coarse sand in a growthchamber with a 14 h photoperiod (25 C, RH 60 %) followedby IO h of darkness (20 C, RH 80 %). Light (250 pmol . m-*s- PPF) was supplied by 150 W mercury lamps (HQI-TS,Osram, Germany). The pots were watered fiv e times a daywith half-strength Hoagland solution.

4.2. Bioassay with epidermal strips. Epidermal strips(IO mm x 5 mm) were peeled from the abaxial surface of theyoungest ful ly expanded leaves of 4 week old plants ofC. communis. The leaves were harvested at the end of thedark period. Opened stomata were obtained by incubatingthe peels for 2 h 30 min at 20 C under a photosynthetic pho-ton flux of 270 pmol . me2 SC in 20 mM KCl, IO mM 2-[N-morpholinolethane sulphonic acid (Sigma), pH 6, aeratedwith CO; free air (-CO,) obtained by passing dry air oversodalime (Soda Asbestos, Prolabo. Paris, France). After-wards, irradiation continued for 2 h under -CO, in the pres-ence of (+/-) cis-trans abscisic acid (ABA; Sigma) at IO or100 nM. The external pH was varied by buffering the bathingsolution at pH 5 (with 10 mM cit rate) and pH 7 (with IO mMHepes) at the beginning of the experiment. It was verifiedthat, in the absence of external ABA, these pH buffers did notmodify the mean stomata1 aperture.4.3. Experiments with Ca + buffers. To buffer cytosolicfree Ca+, EGTA (Sigma) or BAPTA (Sigma) was added tothe bathing solution at the start of the experiment. The 50mM stock solutions of EGTA and BAPTA contained K+ atI53 and 220 mM respectively. Control bathing solutions con-tained the K+ salt of the imino-diacetic acid (Interchim) toad,just their final Kf concentrations at the same values asthose exhibited by the EGTA- and BAPTA-containing solu-tions.4.4. Experiments with protein kinase inhibitors andcalmodulin antagonists. To block protein phosphorylationand Ca*+-calmodulin (CaM) complex dependent processes.the following inhibitors were separately supplied to the bath-ing solution 30 min before applying ABA: the protein kinaseinhibitors H-7. K-252a, KT5926 and ML-7 at the respectiveconcentrations of 20,1, 1 and 20 PM, and the CaM antago-nists W-5 and W-7 at 20 yM. These concentrations wereretained from preliminary dose/response studies. It was veri-fied that, at these concentrations, H-7, K-252a. KT5926.ML-7. W-5 and W-7 alone changed the mean stomata1 aper-ture by less than I.5 pm. These inhibitors were dissolved indimethyl sulphoxyde (DMSO; Sigma), except H-7 whichwas dissolved in distilled water. The control bathing solu-tions contained DMSO at the same concentrations (I 0.1 %v/ v) as the inhibitor-containing solutions. All these inhibitorswere purchased from Biomol Research Laboratories Inc.(Plymouth Meeting, UK).4.5. Experiments with inhibitors of G protein function-ing. To modulate G protein functioning, the following com-pounds were separately added to the bathing solution 30 minbefore applying ABA: the aminosteroid U73 122 and its ana-logue U73343, the G protein antagonist pGlu-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH* (GP Ant-2) and its analogueGP Ant-2A, and mas 17, an inactive analogue of mastoparan.All these modulators were obtained f rom Biomol ResearchLaboratories Inc, (Plymouth Meeting, UK) and used at opti-mal concentrations, retained from preliminary dose/responsestudies. Whils t GP Ant-2A and mas 17 were dissolved in ster-

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ile double distilled water, U73122, U73343 and GP Ant-2were dissolved in DMSO (Sigma), and control bathing solu-tions contained DMSO at the same concentrations (2 0.1 %v/ v) as the U73122-, U73343- and GP Ant-2-containingsolutions.4.6. Data analysis . Stomata1 apertures were measured withan optical microscope (Nikon, Optiphot, Tokyo, Japan) fittedwith a camera lucida and a digitizing table (Houston Instru-ment, Austin, TX) linked to a personal computer (Compaq,Houston, TX). For each treatment. fiv e epidermal strips werefloated on 10 ml of bathing solution and 10 stomata1 aper-tures were measured f rom each epidermal strip. Except whenotherwise noted in the figures, each data point represents themean of 50 stomata1 apertures with the confidence limits tothe mean for o! = 0.05.Acknowledgments. The authors thank Prof. Nam Hai Chua(The Rockefeller Unive rsity , New York, USA) and Dr AndreVermeglio (CEA, Cadarache, France) for commenting on themanuscript.

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