Plant Physiol. (1982) 70, 1079-10830032-0889/82/70/1079/05/$00.50/0

Rapid Changes in the Pattern of Electric Current around the RootTip of Lepidium sativum L. following Gravistimulation'

Received for publication January 18, 1982 and in revised form May 10, 1982

H. M. BEHRENS2, M. H. WEISENSEEL3, A. SIEVERS2Botanisches Institut der Universitat Bonn, D-5300 Bonn 1 (H. M. B., A. S.); and Botanisches Institut derTechn. Universitat Karlsruhe, D- 7500 Karlsruhe (M. H. W.); Federal Republic of Germany

ABSTRACT

Using a highly sensitive vibrating electrode, the pattern of naturallyoccurring electric currents around I-day-old primary roots of Lepidiumsativum L. growing vertically downward and the current pattern followinggravistimulation of the root has been examined. A more or less symmetricalpattern of current was found around vertically oriented, downward growingroots. Current entered the root at the root cap, the meristem, and thebeginning of the elongation zone and left the root along most of theelongation zone and in the root hair zone. After the root was tilted to ahorizontal position, we observed current flowing acropetally at the upperside of the root cap and basipetally at the lower side within about 30seconds in most cases. After a delay of several minutes, acropetallyoriented current was also found flowing along the upper side of themeristematic zone. The apparent density of the acropetal current in theroot cap region increased and then decreased with time. Gravitropiccurvature was first visible approximately 10 minutes after tilting of the rootto the horizontal position. Since the change in the pattern of current in theroot cap region precedes bending of the root and is different for the upperand lower side, a close connection is suggested between the current andthe transduction of information from the root cap to the elongation zonefollowing graviperception in the cap.

Measurements with an extracellular vibrating electrode haverevealed characteristic patterns of self-generated electric currenttraversing individual plant and animal cells (5, 6, 19, 21). Growingpollen tubes and root hairs, for example, produce an electriccurrent which enters at the growing tip and leaves at the basal,nongrowing region of the cell (19, 22). Electric currents and fieldshave also been observed around entire organs, such as roots,hypocotyls, and coleoptiles (10-12, 17, 20). Suggested roles forthese currents in roots are in ion uptake (13) or elongation (2).Around coleoptiles oriented horizontally, electric potentials

have been observed in the form of a transverse polarization, withthe lower side becoming positive (1). However, since this trans-verse polarization has a latent period of 10 to 15 min, it is surelynot related to the graviperception because the presentation timefor gravistimulated plants lies between 12 and 30 s (18). It may berelated to the graviresponse (3, 24). Recently, however, hypocotyl

Supported financially by the Deutsche Forschungsgemeinschaft.2 Present address and address for reprint requests: Botanisches Institut

der Universitat Bonn, Venusbergweg 22, D-5300 Bonn 1, Federal Republicof Germany.

3 Present address and address for reprint requests: Botanisches Institutder Techn. Universitat Karlsruhe, Kaiserstrasse 2, D-7500 Karlsruhe,Federal Republic of Germany.

segments tilted to the horizontal position were reported to undergoa change in surface potential within as short a time as 2 to 3 mi(17).We shall attempt to show that a vertical, freely growing root

has a steady pattern of current and that the pattern changes whenthe root is placed horizontally. Such a change suggests that thecurrent could be involved in the transduction of gravitropic stirn-ulus.

MATERIALS AND METHODS

Growth Conditions and Holding Apparatus for Seedlings. Seedsof Lepidium sativum L. were soaked 30 min in tap water and thenplaced on vertical moist filter paper in a closed container. Theseeds were oriented with their micropyles down so that the rootswould not curve during germination. After 20 h at a temperatureof 23 + 2°C, the primary roots were 6.0 ± 1.2 mm long. Singleseeds were then transferred and fastened with a drop ofwarm agarmedium to a small L-shaped Plexiglas holder which, after a further3.5 h, was clamped in a micromanipulator, avoiding as much aspossible any shaking of the seed. Using the micromanipulator, theroot was placed in the desired orientation in relation to gravityand the measuring electrode.Measurement of the Natural Electric Currents. The natural

electric current of the growing roots was measured in an aqueousmedium, after allowing the roots to adapt 30 min to the medium.The medium used was an air-saturated APW4 containing 1.0 mMNaCl, 0.1 mm KC1, 0.1 mm CaCl2, and 1.0 mm Tris. The mediumhad a specific resistivity of 3.7 to 4.3 x 103 ohm cm, a pH of 7.2to 7.4, and a temperature of 200 to 23°C. The strength and patternof the electric current were measured with an advanced version ofthe vibrating electrode (5; A. Dorn and M. H. Weisenseel, inpreparation). The measuring electrode consisted of a metal-filledmicropipet with a platinum-black ball of 30 ,um in diameter at itstip. A concentric platinum-black reference electrode was located5 mm behind the tip. Using a piezoelectric element, this combi-nation electrode was vibrated, only horizontally, at a frequency of460 Hz and an amplitude of 32 ,um. The vibration transformedany DC-voltage difference between the two endpoints of vibrationinto a sinusoidal AC-voltage which was measured with the aid ofa lock-in amplifier (model 129 A, with phase control; PrincetonApplied Research). Because the electric field (E) is approximatelyconstant over the small vibration distance, the local current density(I) in the direction of vibration can be calculated from themeasurement of the local voltage difference (A V), the specificresistivity of the medium (p), and the amplitude of the vibration(d): I = E/p = A V/p d. The calculated current density may beconverted to ion flux by division with the Faraday constant: ie. 1,uamp cm2 corresponds to 10 pmol cm-2 s-1 for monovalent ions.

4 Abbreviation: APW, artificial pond water.

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Plant Physiol. Vol. 70, 1982

(As usual, the direction of current flow is defined as the directionof movement of positive charge.)Measurement Positions. The positions for measurement were

located 100 pun apart along the long axis of the root and with thehelp of two micromanipulators (one carrying the vibrating elec-trode and one to which the seedling was attached), maintainedwithin a range of about 3 ,tm. The positions of the electrode androot were observed from below with an inverted microscope(Zeiss) and from the side with a horizontally mounted stereomicroscope (Leitz). The distance between the midpoint of thevibrating electrode and the root surface was approximately 70 ,umin each measurement position. For each position, measurementswere made on both sides of the root in the same transverse planeof the root. In the vertical orientation, these measurements weremade on two opposite flanks of the root. The electrode vibratedperpendicular to the root surface and therefore measured theinward or outward component of positive current flow. In thehorizontal orientation, measurements were made on the upperand lower sides of the root. For technical reasons, the electrodecould only be vibrated horizontally; therefore, it vibrated parallelto the surface of the horizontal roots. This is the reason for thefact that only the acropetal or basipetal component of current nearthe surface of these roots was measured (see "Discussion"). Ineach position, the voltage difference was measured for severalseconds to several minutes and measurements were repeated sev-eral times in succession.Root Growth, Graviresponse, and Root Anatomy. The growth

in length of the root during current measurements was observedusing an ocular micrometer in the stereo microscope. The currentzones were compared with the anatomically and functionallydifferent zones in primary roots. The elongation region duringnormal vertical growth and gravitropic growth were determinedby application of starch grains to the root surface (7). Rootanatomy was studied in KMnO4-fixed and epoxy-embedded sec-tions (7, 14).

RESULTS

Anatomical and Functional Segmentation of the Primary Rootof Lepidiwmn A median longitudinal section through the tip of avertically grown 24-h-old primary root shows three anatomicallyand functionally defined regions. From the tip to the base of theroot, these regions are as follows (Fig. IA). (a) The root cap,which is 120 to 170 Ium long, lies at the tip. Its central region iscalled the statenchyma and contains cells with amyloplasts thatare able to sediment in the gravitational field. The cells also showa striking endomembrane system at their distal ends. The staten-chyma is the site of graviperception (14, 15, 18). (b) Behind theroot cap lies a meristematic zone which extends to about 800 ,mfrom the tip. The cells of this zone are small and rich in cytoplasm,making the region appear dark in the light microscope. Thecontribution of these cells to the total elongation of the root isonly about 10%o to 13% (7). (c) The elongation zone begins about800,tm basipetal to the root tip and reaches up to the root hairzone, approximately 3,000 um from the tip. The zone wheremaximal elongation of cells occurs lies between 1,500 and 2,400Mum. This root zone, which is responsible for about 55% to 60% ofthe total root elongation, was recognized by observing the rate ofseparation of particles applied to the root surface (7).At the beginning of the measurements, the 23.5-h-old seedlings

had roots of an average length of 7.5 + 1 mm. The growth ratewas 2 to 22 Mm min' and was unaltered during the 30-minadaption in APW. A decrease in the average growth rate to 1 to9 Mim min- was first seen after 3 to 4 h in APW. The growth ofroot hairs and the development ofnew root hairs was not inhibitedin APW during the time of the experiments.The analysis of root growth of the two sides of the root during

the first 20 min following tilting of the root to the horizontal

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FIG. 1. Anatomical and functional organization of the tip of a 24-h-oldLepidium root (A) and diagram of the qualitative current pattern of aLepidium root growing vertically downward (B). A, the micrograph of amedian longitudinal section ofa vertically grown primary root shows threedifferent regions along the longitudinal axis. (a) Zero to about 170 Pm;root cap with centrally located statenchyma, the site of graviperception.(b) About 170 to about 800 Mm; meristematic zone with cell divisions. (c)About 800 to about 3,000 Mm; elongation zone; the maximal rate ofelongation occurs between approximately 1,500 and 2,400,um (micrographcourtesy of R. Kruft). B, Information for diagramming the current patterncomes from measurements of the current direction and density at positionsapproximately 70 pm above the root surface of 26 roots. Arrows (I)indicate the direction of current flow, i.e. the direction of movement ofpositive ions. The direction of the gravity vector (g) is indicated by a widearrow ( I ). A pair of solid circles (@0) symbolizes the tip of the vibratingelectrode, the direction of vibration in relation to the root surface, and atypical measurement position. The orientation of the electrode's shaft isindicated by the vertical bars on the solid circles.

position showed that the root cap and the adjacent meristematiczone were not involved in formation of a curve. The differentialgrowth of the two sides of the elongation zone usually began notearlier than 7 to 10 min after tilting the root (Fig. 2B) andremained restricted to the elongation zone.The Natural Electric Current of Vertically Growing Lepidium

Roots. Measurements on both sides ofthe roots at 100-gm intervalsalong the root revealed that roots growing exactly vertically down-ward are surrounded by an approximately symmetrical electricfield. In Table I, values are given for the apparent current densityat each level of measurement. (The current density is called'apparent' because only its magnitude normal to the surface, invertical roots, or parallel to the surface, in horizontal roots, wasdetermined during the present measurements.)Only one value is given for each level since the values for the

opposite sides of the root at a given level were always approxi-mately equal. In the longitudinal direction, three zones defined bythe current direction could be distinguished (Fig. IB; Table I). (a)An inward current was measured at the surface of the root cap,the meristematic zone, and the beginning of the elongation zone.The maximal apparent current density of about 1.2 ,Ramp cm-2, at70Mum from the surface was located 800± 300Mum basal to the tip.(b) A 100 to 300 pm long zone (1500-1600 ,um from the tip) of'zero' current, i.e. a zone in which no or only negligible currentcould be measured normal to the surface, was found immediatelybasipetal to the zone ofinward current. The measurement of 'zero'current indicates that, in this zone, current flows parallel to theroot surface so that the lines of the electric field run perpendicularto the direction of vibration of the electrode, and are therefore not

1080 BEHRENS ET AL.

ROOT CURRENT AND GRAVIPERCEPTION

Table I. Current Density and Direction of the Natural Electric Current at the Tip ofa Representative Lepidium RootThe values come from measurements made either perpendicular to the surface (vertical roots) or parallel to the surface (horizontal roots). The values

at positions every 100,m along the root, beginning at the tip, are presented. The values show only small fluctuations during the 2- to 3-h observationperiod. For the horizontal root, the values for current density and direction are presented separately for each side.

Vertical Positiona Horizontal Position

Positin.Upper side Lower side Time afterPosition Current Current Horizontal

density direction Current Current Current Current Positioningdensity direction density direction

,uM Aamp cm-2 pamp cm-2 ,pamp cm-2 min0 0.00 0.34 Acropetal I

100 0.05 Inward 0.57 Acropetal 0.50 Basipetal 21.72 Acropetal 0.98 Basipetal 5

200 0.19 Inward 1.90 Acropetal 1.30 Basipetal 7300 0.26 Inward 2.19 Acropetal 1.20 Basipetal 9400 0.53 Inward 1.11 Acropetal 11500 0.95 Inward 0.52 Acropetal 12600 1.00 Inward 0.52 Acropetal 14700 1.11 Inward 0.45 Acropetal 18800 1.13 Inward 0.40 Acropetal 19900 0.98 Inward 0.30 Basipetal 21

1,000 0.98 Inward 0.85 Acropetal 221,100 0.98 Inward1,200 0.85 Inward 0.86 Acropetal 231,300 0.74 Inward 0.86 Acropetal 251,400 0.40 Inward1,500 0.00 Parallel1,600 0.00 Parallel1,700 0.10 Outward1,800 0.42 Outward1,900 0.46 Outward2,000 0.48 Outward

a Values are entered for only one of the root flanks since the opposite flanks showed no significant difference.

detected. (c) Adjacent to the zone of zero current was a zone withan outward current. This current increased in apparent densityfrom the apical to the basal part of the zone. The measureddensities, from 0.2 to 0.8 ,uamp cm-, were lower on the averagethan in the zone of inward current. The zone of the outwardcurrent began at 1700 ± 300 pm basipetal to the root tip andapproximately 300 ,um in front of the root hair zone. The zone ofoutward current became displaced in the acropetal direction dur-ing a 3-h measurement period, as did the region of root hairinitiation.The fluctuations in apparent current density at individual po-

sitions within individual roots were small and showed no partic-ular pattern. There was considerable variation between differentroots, however. The range in values for the maximal apparentcurrent density of inward current was from 0.5 to 3.4 ,uamp cm-.Roots with a higher level of current were also found to have amore rapid rate of growth. In spite of the variation in currentdensity, all roots measured had current moving inward in apicalregions and outward in basal regions of the root tip, and thus, thegeneral current pattern was identical for all roots growing exactlyvertically downward.

Figure lB shows a qualitative and representative current patternaround a vertically growing root. This pattern was drawn on thebasis of a total of 1,200 measurements near the surface of 26different roots.The Natural Electric Current of Horizontally Oriented Lepidiwn

Roots. With the occurrence of circumnutation in vertically grow-ing roots, we noticed a slight change in the symmetry of thecurrent pattern at the root cap and meristem (data not shown). Toexamine precisely the influence of root orientation on the currentpattern, we first measured the current pattern around verticallygrowing roots and then tilted them to the horizontal position.

Beginning as quickly as possible, i.e. approximately 30 s aftertilting the root, current measurements were taken at positionsbetween 0 and 300 ,um from the tip. Measurements at thesepositions were made in a different order for different roots, andthen the measurements in other positions were made at periodictime intervals. Simultaneously with these surrent measurements,we observed the gravitropic curvature using the horizontal micro-scope. The current densities and directions along the upper andlower surface of a representative root during the first 25 minfollowing exposure to the horizontal position are shown in TableI.As early as 30 s after tilting the root, we observed current

flowing in the acropetal direction at the upper side of the rootwhich rapidly increased in apparent density during the first min-utes. Current flowing in the basipetal direction was observed atthe lower side of the root throughout the time of measurements.The apparent density of this basipetal current increased especiallyin the positions between 100 and 300 ,um, where it reached a levelof up to 10 times that in the vertical root (Table I). When thedirection and density of the current at the upper side were followedduring the first 25 min of horizontal orientation at three selectedpositions corresponding to the functionally different regions of theroot, the root cap (statenchyma), meristem, and elongation zone(1,800 ,im), considerable changes could be measured in these threeregions (Fig. 2B). The current density of the acropetally flowingcurrent first increased rapidly in the root cap region and then after10 min decreased. At the meristem, a change in the direction ofcurrent from basipetal to acropetal and an increase in currentdensity was seen after 8 min. However, at the 1,800 ,um position,no change in the direction or density of acropetally flowing currentwas measured even after 20 min. At 7 to 12 min after tilting to thehorizontal, the root began to curve. Similar changes were seen in

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Plant Physiol. Vol. 70, 1982

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FIG. 2. A, Values for current direction and apparent density at three selected measurement positions near a representative vertically growing root.The selected measurement positions correspond to the functionally different regions of the root tip: root cap (U, statenchyma), meristem (O), and theelongation zone (E, 1,800 .tm). Each bar represents the apparent current density (+SE) of the measurement positions. The root tip is characterized byan inward current in the root cap region and meristem and an outward current in the basal region of the elongation zone. B, Measurements as in A near

the upper side of a representative horizontally growing root, including measurements of the graviresponse. The root cap and meristematic regions showan acropetal current of increasing (and for the root cap later, decreasing) apparent density. The basal region of the elongation zone shows an acropetalcurrent of constant apparent density during the measurement period. The graviresponse (curvature in degrees, O---0) of the same root begins 9 minafter the root has been tilted. C, Schematic drawing of the measured current directions on the upper and lower side of horizontal roots about 30 s (t,)and 3 min (t2) after tilting the root from the vertical to the horizontal. The drawing was made on the basis of a total of 700 measurements from 16different roots. (ez), Elongation zone.

the other 15 roots investigated. As early as 30 s after tilting theroot, we sometimes detected an acropetal current at the root capregion (Fig. 2C). Some roots showed a basipetal current at thistime and only later (but always by 3 min) an acropetal current.The meristem region showed a basipetal current at 30 s and an

acropetal current by 3 min. The root cap and meristem regions onthe lower side of the root had a basipetal current only. In the basalregion of the elongation zone, always an acropetal current wasmeasured on both upper and lower sides.

DISCUSSION

Measurements of the direction and magnitude of the electricfield around primary roots of Lepidium growing vertically down-ward show an approximately radially symmetrical pattern of ioniccurrent surrounding the root. Histological examination of roots ofthe same age allow an assignment of parts of the current to theanatomically and functionally different zones of the root. Currentflows into the root cap, meristematic zone, and beginning of theelongation zone. Current leaves the root in the region from thezone of rapid elongation up to and including the root hair zone.The present measurements indicate that an absolute current of atleast 30 namp flows through the root tip of Lepidium. Since the

current pattern can be seen as a color pattern on agar mediumcontaining bromocresol purple, H+ ions are probably the majorcomponent of the current (20).Within 3 min after tilting the root to the horizontal, an acropetal

current could be measured above the root cap and an increasingbasipetal current on the lower side (Table I; Fig. 2C). An acropetalcurrent also appeared in the meristematic zone after a delay of Ito 2 min. These currents are thus arranged asymmetrically at theroot cap and meristem region, in contrast to the symmetricalcurrent pattern seen around vertical roots. In the basal region ofthe elongation zone, an acropetal current flowed along both upperand lower sides of the root and remained unchanged in directionand density for the full 20-min measurement period followinggravistimulation. A differential elongation, serving to return theroot tip to the vertical position, was observable 7 to 12 min aftertilting the root (8).The measurements of asymmetric currents in the root tip region

following horizontal positioning of roots seem to indicate that a

change in the current pattern has occurred. Two possible expla-nations exist for the origin of the acropetal and basipetal currents.(a) The direction of the current on the upper side of the root tiphas reversed polarity, i.e. instead of current entering this region,

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1082 BEHRENS ET AL.

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ROOT CURRENT AND GRAVIPERCEPTION

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FIG. 3. A hypothetical current pattern of 24-h-old Lepidium roots,tilted horizontally for 20 min. The current pattern is based on a possibleinterpretation of the measurements of acropetal and basipetal currents.This figure allows a direct comparison of pattern for horizontal roots withthat for vertical roots (Fig. 1B).

current leaves it. No such reversal from sink to source then seemsto have occurred on the lower side where current flows in abasipetal direction as expected from the pattern in vertical roots.However, the fact that current density increases on the lower sidesuggests that the lower side has also changed following gravisti-mulation, and part of the current entering the root cap region onthe lower side may come from the current leaving the upper sideof the root cap, rather than from the base of the lower side as inthe vertical root. The pattern could be as diagrammed in Figure3. (b) The second possibility is that the path of the current on theupper side becomes constricted and drawn close to the surface ofthe root, so that acropetal components appear in the current nearthe root tip. This explanation of an acropetal current at the tipwould require either an increase in magnitude of the current sinkand/or an increase in conductance of the medium near the rootsurface. We feel that the second possibility is less likely than thefirst one. Measurements with a probe vibrating vertically willshow which explanation is correct. An indication that the acropetalcurrent seen near horizontal root caps is actually an outwardcurrent comes from measurements on vertical roots undergoingstrong circumnutation, and thus having root caps brought awayfrom the vertical position. With these roots, we measured anoutward current with the vibrating electrode constantly kept per-pendicular to the root surface (data not shown).The current pattern shown in the present paper for vertical

Lepidium roots is qualitatively similar to the current pattern foundin vertical roots of bean with surface electrodes (10, 11).A comparison of the electrical events in Lepidium with the time

course of curvature shows that the changes in current patternoccur before a visible curvature. Observation of the correspond-ence between the functional segmentation of the root and theregion ofchanges in current allow us to suggest a possible functionfor the current. The very rapid change at the root cap, producingdifferent patterns at the upper and lower sides of the root cap,suggests an involvement of the current with graviperception. Whenamyloplasts which rest on the ER move away from the ERfollowing gravistimulation (18), a change in the flow of ionsthrough the endomembranes could result. This change could havean effect across the plasmalemma and through the apoplast, outto the surrounding medium. The rapid changes in current supportthe idea that such an ionic transduction mechanism is involved ingraviperception.

Since in the root the sites of graviperception and graviresponseare spatially separated, it is necessary that information is translo-cated longitudinally. An involvement of ABA and IAA has beendiscussed in this connection (4, 9, 23). Whether ABA or another

growth inhibitor (16) plays a primary role in transporting infor-mation remains unclear. A differential transversal redistributionof ABA of approximately 11% could be measured, using radio-active labeling, only at the earliest 1 h after tilting bean roots tothe horizontal position (4).As our data show, the current pattern of root tips is measurably

altered and this in most cases within about 1 min after tilting rootsto the horizontal position. The transfer of information by electriccurrents thus appears to be a further possibility. Because electriccurrent always flows in circles, a current measured outside theroot indicates the existence of a current flowing in the oppositedirection inside the root. A consequence of this internal currentcould be the production of a concentration gradient of ions and ofan electric field. This field and/or the concentration differencescould then produce, for example, a redistribution of specificcarriers for hormone transport.

Acknowledgments-We thank Dr. A. Dorn for help with the vibrating electrodeand Dr. J. M. Lang for translating the manuscript and for helpful discussions.

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