H -ATPase Activity from Storage Tissue of Beta vulgaris'

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1 Plant Physil. (1985) 78, /85/78/95/5/$l./ H -ATPase Activity frm Strage Tissue f Beta vulgaris' III. MODULATION OF ATPase ACTIVITY BY RACTION SUBSTRATS AND PRODUCTS Received fr publicatin September 2, 198 and in revised frm March 15, 1985 ALAN B. BNNTT*2, SHARMAN D. O'NILL3, MARIANN ILMANN, AND ROGR M. SPANSWICK Sectin fplant Bilgy, Divisin fbilgical Sciences, Crnell University, Ithaca, New Yrk 1853 ABSTRACT Tw distinct membrane fractins cntaining Ht-ATPase activity were prepared frm red beet. One fractin cntained a H'-ATPase activity that was inhibited by NO3- while the ther cntained a H'-ATPase inhibited by vanadate. We have previusly prpsed that these H'- ATPases are assciated with tnplast (N3-sensitive) and plasma membrane (vanadate-sensitive), respectively. Bth ATPases were examined t determine t what extent their activity was influenced by variatins in the cncentratin f ATPase substrates and prducts. The substrate fr bth ATPases was MgATP-, and Mg2" cncentratins in excess f ATP had nly a slight inhibitry effect n either ATPase. Bth ATPases were inhibited by free ATP (ie. ATP cncentratins in excess f MgW) and ADP but nt by AMP. The plasma membrane ATPase was mre sensitive than the tnplast ATPase t free ATP and the tnplast ATPase was mre sensitive than the plasma membrane ATPase t ADP. Inhibitin f bth ATPases by free ATP was cmplex. Inhibitin f the plasma membrane ATPase by ADP was cmpetitive whereas the tnplast ATPase demnstrated a sigmidal dependence n MgATP`- in the presence f ADP. Inrganic phsphate mdertely inhibited bth ATPases in a nncmpetitive manner. Calcium inhibited the plasma membrane but nt the tnplast ATPase, apparently by a direct interactin with the ATPase rather than by disrupting the MgATP- cmplex. The sensitivity f bth ATPases t ADP suggests that under cnditins f restricted energy supply activity may be reduced by increases in ADP levels rather than by decreases in ATP levels per sc. The sensitivity f bth ATPases t ADP and free ATP suggests that mdulatin f cytplasmic Mg2 culd mdulate ATPase activity at bth the tnplast and plasma membrane. lectrgenic H+ transprt is thught t be the primary transprt event ccurring acrss the plasma membrane and tnplast f plant cells. Prtn-translcating ATPases have been identified in bth islated plasma membrane and tnplast vesicles f red beet (5). These H+-ATPases are mst likely respnsible fr the majrity f active H+ transprt acrss these membranes. arly attempts t relate the activity f electrgenic H+ transprt acrss 'Supprted by United States Department f Agriculture Cmpetitive Grants Prgram grant 8 1-CRCR and Natinal Science Fundatin grant PCM Present address: Mann Labratry, Department f Vegetable Crps, University f Califrnia, Davis, CA Present address: Plant Grwth Labratry, University f Califrnia, Davis, CA Present address: Advanced Genetic Sciences, Inc., 671 San Pabl Avenue, Oakland, CA the plasma membrane t levels f cytplasmic ATP were nly partially successful (13). While experiments indicated that ATP is indeed the surce f energy fr H+ transprt, the lack f cmplete crrespndence between ATP levels and electrgenic H+ transprt activity suggested that regulatry mechanisms ther than energy supply (i.e. ATP levels) were perative in cntrlling H+ transprt (13). Similar cnclusins were als inferred regarding the activity f H+ transprt acrss the tnplast, since the bserved gradients f &AH' in viv are generally far frm the thermdynamic equilibrium predicted fr a H+-ATPase with a H+/ATP cupling stichimetry f 2 (6). Althugh it nw seems apparent that H+ transprt is nt regulated by energy supply per se, it is likely that H+-ATPase activity wuld be respnsive t sme cmpnent(s) fthe cellular energy charge since these ATPases may accunt fr a significant prprtin f the turnver f cellular ATP. In rder t begin t assess the influence fcellular cnstituents which may cntribute t regulatin f plasma membrane and tnplast H+-ATPase activity in viv, we have examined the effects f reactin substrates and prducts n H+-ATPase activity assciated with islated plasma membrane and tnplast vesicles frm red beet. MATRIALS AND MTHODS Membrane Preparatin. Membranes were prepared frm the strage tissue f red beet as previusly described (5). Fractins enriched in NO3-sensitive and vanadate-sensitive ATPase activity were cllected frm the 16/26% and 3/% interfaces, respectively, f a discntinuus sucrse gradient. Apprximately 8 t 9% f the ATP hydrlyzing activity in these tw fractins is attributable t the activity f H+-translcating ATPases which we prpse are f tnplast (NOC3-sensitive ATPase) r plasma membrane (vanadate-sensitive ATPase) rigin (5). ATPase Assay. ATPase activity was measured at 25C fr 3 min with 1 t 1,g prtein per assay. The reactin was carried ut in a vlume f.5 ml cntaining 5 mm KCI, 3 mm Tris/ Mes, 2 Mm gramicidin, with cncentratins ftris-atp, MgSO, and ther additins as indicated in the text r figure legends. Phsphate was determined by the methd f Ames (2). Reactin blanks (i.e. n enzyme) were prepared fr each treatment and subtracted t calculate the ATPase activity. High cncentratins f ATPfs interfered with clr develpment using the Ames reagent. In the presence f high cncentratins f ATPf and in the presence f Pi, ATPase activity was measured by cupling ATP hydrlysis t NADH xidatin with P-enlpyruvate/pyruvate kinase and lactate dehydrgenase and mnitring NADH xidatin spectrphtmetrically (A3) (6).The reactin was carried ut in a vlume f 1. ml cntaining 5 mm KCI, 3 mm Tris/Mes, 5 mm MgSO,.2 mm P- enlpyruvate,.15 mm NADH, 12 units lactate dehydrgenase, and 7 units pyruvate kinase. Neither high cncentratins fatpf 'Abbreviatin: ATPf, free ATP.

2 96 nr Pi interfered with reactins cupling ADP prductin t NADH xidatin. The assay ph was adjusted t 6.5 fr plasma membrane fractins and 7. fr tnplast fractins. MgATP'-, Free ATP, Free Mg2e Calculatins. MgATP2-, free Mg2+, and ATPf(ATP- + HATP3- + H2ATP2-) were calculated using the iterative prcedure f Strer and Crnish-Bwden (1) using assciatin cnstants published by Alberty (1). RSULTS BNNTT T AL. Bth plasma membrane and tnplast ATPase activities have been shwn t be Mg2" dependent (3, 16). Figure 1 shws the cncentratin dependence f bth plasma membrane and tnplast ATPases (Fig. IA) fr Mg2" when assayed in the presence f 5 mm ATP. The results in Figure 1 are similar t thse f Balke and Hdges (3), and Walker and Leigh (16) fr plasma membrane and tnplast ATPases, respectively. These results suggest that MgATP2- is the substrate fr bth ATPases and further indicate that increasing cncentratins f excess Mg2" have nly a slight inhibitry effect n ATPase activity. This slight inhibitin by high Mg2" may result frm the frmatin f Mg2ATP, and cnsequent reductin in MgATP2- cncentratin (15). When Mg2" was held cnstant and the cncentratin dependence f bth plasma membrane and tnplast ATPases fr ATP was determined, a strikingly different result was bserved (Fig. 2, A and B). At cncentratins f ATP exceeding the fixed Mg2' cncentratin (either 2.5 r 5. mm), ATP was strngly inhibitry. Since ATP did nt inhibit ATPase activity at cncentratins equal t r belw the fixed cncentratin f Mg2", it seemed likely that the inhibitry species was uncmplexed, r ATPf. A similar result was previusly reprted fr the plasma membrane ATPase f at rts (3); hwever, a lack f sensitivity t ATP has been reprted fr the sugarcane tnplast ATPase (15). The inhibitin f bth ATPases reprted here des nt result frm an effect f ATP n ur determinatin f Pi, since these ATPase assays were perfrmed using an enzymically cupled assay ("Materials and Methds") that measures the prductin f ADP and is nt effected by ATP. Cncentratins f ATPf were calculated at each cncentratin f ATP and Mg2' and the ci - ;7 X) 6 ' q-, 2 1 Mg F. a.' - O' 1.._._._._../ _ -~O.1 ~~~~~. g PLASMA MMBRAN 6 / Ina- Mg:ATP zt aa U. I FR ATP a)k9,- 2- / M q: ATF 1 /IATP MgSO FIG. 1. A, ATPase activity f bth tnplast and plasma membrane ATPases measured in the presence f 5 mm ATP and increasing cncentratins f MgS. ATPase activity was assayed by mnitring the release f Pi as described in "Materials and Methds". B, Cncentratins f free Mg2+ (Mg2`f), MgATP2-, and free ATP (ATPf = ATP- + HATP3- + H2ATP2-) at the indicated cncentratins f MgSO and 5 mm ATP PLASMA b 2 8 ZL C- D 2 ( I2 335 Plant Physil. Vl. 78, ;l mm-, 5 5mM\ mm ' ATP FIG. 2. ATPase activity f bth plasma membrane and tnplast ATPases measured in the presence f 2.5 r 5 mm MgSO and increasing cncentratins f ATP. ATPase activity was assayed by cupling ATP hydrlysis t NADH xidatin as described in "Materials and Methds". a >,2,, r ~~~MMBRAN - e 9 \ \ Mg2 = I 2.5mM 8 a.8~~~~s PPLASMA MMBRAN FIG. 3. ATPase activity f bth tnplast and plasma membrane ATPases as a functin f free ATP. Data is repltted frm Figure 2 after calculating the cncentratin ffree ATP at each cncentratin fmgso and ATP. data in Figure 2, A and B, repltted t shw the cncentratin dependence f ATPase inhibitin by ATPf (Fig. 3). It is apparent frm this plt f the data that the plasma membrane ATPase was mre sensitive t ATPfthan was the tnplast ATPase. The cncentratin f ATPf giving half-maximal inhibitin (I5) was 2.1 and.5 mm fr the plasma membrane and tnplast ATPase, respectively. T evaluate the mechanism f ATPase inhibitin by ATPf, the MgATP cncentratin dependence fr bth ATPases was determined in the presence f increasing ATPf (Fig. ). The plasma membrane ATPase was inhibited by ATPf at all MgATP cncentratins (Fig. A). Althugh the effect f ATPf n the tnplast ATPase was less prnunced, ATPf apparently stimulated ATPase activity at lw cncentratins f MgATP and inhibited activity at high MgATP cncentratins (Fig. C). Hanes-Wlf plts f the data in Figure A (Fig. B) and Figure C (Fig. D) indicated that inhibitin f ATPase activity by ATPf was cmplex. A differential effect f ATPf n the plasma membrane and tnplast ATPase was apparent in that the Km fr MgATP increased with increasing ATPffr the plasma membrane ATPase, but decreased with increasing ATPf fr the tnplast ATPase. (Fig., B and D). Since it was apparent that ATPf was much mre inhibitry f O -*I_ M

3 MODULATION OF ATPase ACTIVITY PLASMA MMBRAN (C) r, 2,/ O 6 > A 2 2 7A a 2 6 TO NO PLAST FR ATP A 3 C., 5 PLASMA MMBRAN A\ I5 = 2.5 m M \ \ 1 _ O.I2.1 O. a. 8.8 Vmax (s&(m)~ml P1/mg-hr).6~~~~~~~~~~ A ~~~ I5=.75 mm \ 3 - \ Mg :ATP FIG.. MgATP cncentratin dependence fbth plasma membrane (A and B) and tnplast (C and D) ATPases at increasing cncentratins f free ATP. ATPase activity was assayed by cupling ATP hydrlysis t NADH xidatin as described in "Materials and Methds". and (D) shw Hanes-Wlf plts f the data in and (C). t m -B ' 7 a _ 2 _ 6~ / / ll~ //z * // *S * * PLASMA MMBRAN 1 _ \X> 2 ADP FIG. 6. ATPase activity f bth plasma membrane and tnplast ATPases in the presence fincreasing cncentratins fadp. ATPase activity was measured in the presence f 5 mm ATP and either 5 mm () r 1 mm () MgSO. ATPase activity was assayed by mnitring the release f Pi as described in "Materials and Methds". r l I u I Km -.6 L).. - U, _, - -~~~~~ _ / / /~~~~~ -~~~~~~~~.1/,., 2 Mg:ATP FIG. 5. MgATP cncentratin dependence f bth tnplast and plasma membrane ATPases assayed in the presence f a cnstant 2-mM excess Mg2". ATPase activity was assayed by mnitring the release f Pi as described in "Materials and Methds". than free Mg2" fr bth ATPases, the cncentratin dependence fr MgATP was determined by increasing MgATP cncentratin in the presence f a cnstant 2 mm excess f Mg2" (Fig. 5). When assayed under these cnditins, bth ATPases shwed simple hyperblic kinetics with a Km Of.68 and.2 mm fr the plasma membrane and tnplast ATPase, respectively. In ther experiments the Km fr the plasma membrane ATPase ranged frm.56 t.83 mm and the Km fr the tnplast ATPase frm.2 t.58 mm. In general, the affinity f bth ATPases fr MgATP was similar enugh that this characteristic is nt useful in distinguishing these H+-ATPases; nr des it suggest that these ATPases wuld shw a differential respnse t reductins in MgATP cncentratins in viv. Since reductins in ATP levels in viv may be accmpanied by increases in ADP levels (1), we examined the effect f ADP n the activity f bth plasma membrane and tnplast ATPases (Fig. 6). Because inhibitin f ATPase activity by ADP culd result frm ADP chelatin f Mg2" and cnsequent prductin.2.2. > 9 c * a..8 uc..16- >. (n 2 3.._ Mg: ATP FIG. 7. MgATP cncentratin dependence fbth plasma membrane (A and B) and tnplast (C and D) ATPases at increasing cncentratins f ADP. ATPase activity was assayed by mnitring the release f inrganic phsphate as described in "Materials and Methds". and (D) shw Hanes-Wlf plts f the data in and (C). f ATPf, the effects f ADP were assayed in the presence f equimlar ATP and Mg2" and in the presence f 5 mm excess Mg2e. The inhibitin f bth ATPases by ADP was similar in the presence and absence f excess Mg2, suggesting that ADP directly inhibited ATPase activity, rather than having an indirect effect n the MgATP cmplex. In cntrast t the inhibitry effects f ATPf, the tnplast ATPase was much mre sensitive t ADP than was the plasma membrane ATPase (Fig. 6, A and B) Ṫhe MgATP cncentratin dependence fr bth ATPases was determined in the presence f increasing cncentratins f ADP (Fig. 7). The inhibitry effect f ADP n the plasma membrane ATPase appeared t be largely cmpetitive (Fig. 7, A and B), whereas the inhibitry effect f ADP n the tnplast ATPase was cmplex (Fig. 7, C and D). In the presence f ADP, the tnplast ATPase shwed a sigmidal cncentratin dependence

4 98 BNNTT T AL. n MgATP. This type finhibitin is bserved when the inhibitr interacts with the substrate (1 1) and suggests that under these assay cnditins, at lw MgATP cncentratin, ADP is disrupting the MgATP cmplex and indirectly inhibiting ATPase activity. At higher cncentratins f MgATP where ADP effects n MgATP levels are minimized, inhibitin by ADP appears t be cmpetitive (Fig. 7D) as seen fr the plasma membrane ATPase (Fig. 7B). Cmpetitive inhibitin f the Neurspra plasma membrane ATPase by ADP (7) and deplarizatin f the membrane ptential f internally perfused Chara cells ( 12) has been previusly reprted. The effects f AMP and Pi n ATPase activities were als examined (Figs. 8, 9). AMP nly slightly inhibited the plasma membrane and tnplast ATPase at cncentratins up t 5 mm with the maximum inhibitin being less than 1% (Fig. 8). Pi was slightly mre inhibitry than AMP with maximum inhibitin being 37 and 25% fr the plasma membrane and tnplast ATPase, respectively (Fig. 9). The MgATP cncentratin dependence fr bth ATPases was determined in the presence f and 2 mm Pi (Fig. 1). Hanes- Wlf plts f the data (Fig. 1, B and C) indicated that inhibitin f ATPase activity by Pi was largely nncmpetitive. Since divalent catins ther than Mg26 may interfere with frmatin f the MgATP cmplex, we als examined the effect f Ca2+ n the activity f each ATPase (Fig. 1 1). The plasma membrane ATPase was sensitive t inhibitin by Ca2" with greater than 5% inhibitin bserved at 1 mm Ca2" (Fig. 1 A); similar inhibitin f the at rt plasma membrane ATPase has been reprted (). By cntrast, the tnplast ATPase was largely unaffected by Ca2" with a slight, but reprducible, stimulatin f ATPase activity at lw cncentratins f Ca2" (Fig. 1 1B). This slight stimulatin f activity is similar t that bserved by Du- Pnt et al. (9) in crn rt micrsmal vesicles. Since the assays ~ F 2-35 P(MM) -q & a-,l 1 -/ /; zr ffi a * 5 PLASMA MMBRAN 1m Mg: ATP Plant Physil. Vl. 78, 1985 FIG. 1. MgATP cncentratin dependence f bth plasma membrane (A and B) and tnplast (C and D) ATPases in the presence f r 2 mm Pi. ATPase activity was assayed by cupling ATP hydrlysis t NADH xidatin as described in "Materials and Methds". and (D) shw Hanes-Wlf plts f the data in and (C). 3, \\ S _ \ 5^t) 1 _ 5- PLASMA MMBRAN - 7 I- a. 6i Fb 5-1 ~ 3 _ = --5 -_ ffi 2-_MMBRAN I 2 _TONO PLA ST 2 AMP FIG. 8. ATPase activity f bth plasma membrane and tnplast ATPases in the presence f increasing cncentratins f AMP. ATPase activity was assayed with 5 mm ATP and MgS by mnitring the release f Pi as described in "Materials and Methds". I-,.3 PLASMA MMBRAN INORGANIC PHOSPHAT FIG. 9. ATPase activity f bth plasma membrane and tnplast ATPases in the presence f increasing cncentratins f Pi. ATPase activity was assayed by cupling ATP hydrlysis t NADH xidatin as described in "Materials and Methds". 2 CALCIUM CHLORID FIG. I 1. ATPase activity fbth plasma membrane and tnplast ATPases in the presence f increasing cncentratins fca2". ATPase activity was measured in the presence f 5 mm ATP and either 5 mm () r 1 mm () MgS. ATPase activity was assayed by mnitring the release f Pi as described in "Materials and Methds". perfrmed here were in the presence f gramicidin, this stimulatry effect f Ca2" cannt be related t Ca2+/H' exchange affecting ph gradients but must be due t a direct interactin with the ATPase. Since Ca2" can exert effects n the MgATP cmplex, assays were cnducted in the presence f equimlar Mg2+, and ATP (5 mm each) r in the presence f excess Mg2` (1 mm MgSO, 5 mm ATP). In the presence f excess Mg2+ the MgATP cmplex shuld be stabi 3 against interactins with Ca2+ (i.e. frmatin fcaatp), yet similar results were btained in terms f Ca2' inhibitin f activity. This result indicates the effects f Ca2' are nt related t interactins with MgATP but result frm direct interactins with the ATPases. DISCUSSION As shwn previusly (3, 8, 16) these experiments cnfirm that the substrate fr bth plasma membrane and tnplast ATPases

5 is MgATP. Bth ATPases are inhibited by free ATP and by ADP, althugh the sensitivity f the tw ATPases t free ATP and ADP differs. The plasma membrane ATPase is mre sensitive t free ATP than is the tnplast ATPase and, cnversely, the tnplast ATPase is mre sensitive t ADP than is the plasma membrane ATPase. Inhibitin f a plasma membrane ATPase frm at rts by free ATP has been reprted (3). In this previus wrk, hwever, ATPase activity was measured by a clrimetric determinatin f liberated phsphate. As we, and thers (15), have nted, high cncentratins f free ATP interfere with frmatin f the clred phsphmlybdate cmplex. The results presented here were btained by measuring ATPase activity in an enzyme linked assay that is nt affected by free ATP. Cnsequently, we feel the results presented here demnstrate direct inhibitin f bth ATPases by free ATP. The sensitivity f bth ATPases t ADP suggests that ADP culd play a rle in mdulating ATPase activity in viv. Under cnditins f high energy charge, ADP levels are quite lw in viv but increase in crrespndence with decreasing ATP levels under cnditins f diminished energy supply (1). Inhibitin f H+ transprt activity under cnditins f energy deprivatin may ccur as a direct result f increases in ADP, rather than frm decreases in ATP. Cnsequently, attempts t crrelate H+ transprt activity t ATP levels alne may be cnfunded by changes in ther cmpnents f the cellular energy charge. The membrane ptential f internally perfused Chara cells has been shwn t be a functin f bth ATP and ADP cncentratins, with ATP hyperplarizing and ADP deplarizing the membrane ptential ( 12). These results suggest that the effects fadp n ATPase activity measured in vitr are als manifested in viv and may play an imprtant rle in mdulating H+ transprt activity acrss the plasma membrane and tnplast. The plasma membrane ATPase was sensitive t inhibitin by calcium but the tnplast ATPase was nt. Previus bservatins f Ca2" inhibitin f plasma membrane ATPase activity have been attributed t interference with the enzyme-substrate cmplex. The experiments perfrmed here, in the presence f excess Mg2+, wuld minimize effects f Ca2+ n MgATP levels and indicate that Ca2' directly inhibits the ATPase. The differential MODULATION OF ATPase ACTIVITY sensitivity f the tw ATPases t Ca2" is ne distinguishing characteristic f these ATPases, yet the cncentratins f Ca2" (>.1 mm) required fr inhibitin are quite high and unlikely t be f physilgical significance. LITRATUR CITD ALBRTY RA 1968 ffect fph and metal in cncentratin n the equilibrium hydrlysis fadensine triphsphate t adensine diphsphate. J Bil Chem 23: AMS BN 1966 Assay f inrganic phsphate, ttal phsphate and phsphatases. Methds nzyml 8: BALK N, TK HDGS 1975 Plasma membrane adensine triphsphatase f at rts. Activatin and inhibitin by Mg2 and ATP. Plant Physil 55: BALK N, H Sz, RT LONARD, TK HDGs 197 Catin sensitivity f the plasma membrane ATPase f at rts. In J Dainty, U Zimmermann, eds, Membrane Transprt in Plants and Plant Organelles. Springer-Verlag, Berlin, pp BNNIT AB, SD O'NILL, RM SPANSWICK 198 H-ATPase activity frm strage tissue f Beta vulgaris. I. Identificatin and characterizatin f an anin-sensitive H+-ATPase. Plant Physil 7: BNNrr AB, SPANSWICK RM 198 H+-ATPase activity frm strage tissue f Beta vulgaris. II. H+/ATP stichimetry f an anin-sensitive H+-ATPase. Plant Physil 7: BROOKR RJ, CW SLAYMAN 1982 Inhibitin f the plasma membrane H+- ATPase f Neurspra crassa by N-ethylmaleimide. J Bil Chem 257: CALDWLL CR, A HAUG 198 Kinetic characterizatin f barley rt plasma membrane-bund Ca2+- and Mg2e+dependent adensine triphsphatase activities. Physil Plant 5: DuPNT FM, DL GIORGI, RM SPANSWICK 1982 Characterizatin fa prtntranslcating ATPase in micrsmal vesicles frm crn rts. Plant Physil 7: ROBRTS JKM 198 Study f plant metablism in viv using NMR spectrscpy. Annu Rev Plant Physil 35: SGL IH 1975 nzyme Kinetics. Jhn Wiley & Sns, New Yrk, p SMrrH PT, NA WALKR 1981 Studies n the perfused plasmalemma f Chara crallina. I. Current-vltage curves: ATP and ptassium dependence. J Membr Bil 6: SPANSWICK RM 1981 lectrgenic in pumps. Annu Rev Plant Physil 32: STORR AC, A CORNISH-BwDN 1976 Cncentratin f MgATP1- and ther ins in slutin. Bichem J 159: THM M, KMOR 198 ffect f magnesium and ATP n ATPase f sugarcane vacules. Planta 161: WALKR RR, RA LIGH 1981 Characterisatin f salt-stimulated ATPase activity assciated with vacules islated frm strage rts f red beet (Beta vulgaris L.) Planta 153: 1-19

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