MEASUREMENT OF THE TRANS-ROOT ELECTRICAL POTENTIAL OF PLANTS GROWN IN SOIL
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1 New Phytol. (1972) 71, MEASUREMENT OF THE TRANS-ROOT ELECTRICAL POTENTIAL OF PLANTS GROWN IN SOIL BY A. Q. ANSARI* AND D. J. F. BOWLING Department of Botany, University of Aberdeen {Received % June 1971) SUMMARY Electrical potential differences between the soil and the exuding xylem sap of detopped sunflower plants grown in potting compost were measured. The concentrations of some of the major nutrient ions in the soil water and in the xylem sap were determined, enabling the driving forces on the ions to be calculated. The anions, Cl, NO3 and SO4, appeared to be moving from the soil into the sap against the electrochemical potential gradient indicating active transport. There was also evidence that K and Na were actively transported into the xylem. These results are discussed in relation to those obtained with plants grown in water culture. They suggest that this could be a useful method for studying salt uptake by plants growing in the field. INTRODUCTION A number of workers have measured the electrical potential difference between the xylem exudate and the bathing solution of roots grown in water culture (Bowling and Spanswick, 1964; Bowling, Macklon and Spanswick, 1966; Bowling, 1966; Sobey, MacLeod and Fensom, 1970; and others). The magnitude of the potential difference, which appears to depend mainly upon the concentration of potassium in the bathing solution, ranges from 100 mv (xylem sap negative with respect to the bathing solution) to 20 mv (xylem sap positive). If the concentrations of a particular ion in the xylem sap and the external solution as well as the electrical potential difference are known it is possible to calculate the electrochemical potential gradient for the ion. Movement of ions against the electroi:hemical potential gradient is one criterion for active transport. In this paper we describe experiments which extend this approach to the study of 'on transport in sunflower plants grown in potting compost. MATERIALS AND METHODS Sunflower plants {Helianthus annuus tall single variety) were grown in large plastic pots (23 cm diameter), one plant to a pot in either Levington or John Innes No. 2 potting tonipost. They were grown in a growth room at 25" C in continuous light (approximately ''j.ooo lux) until they were five weeks old. The plants in Levington compost were Watered regularly with a proprietry plant food (Liquinure) while those in John Innes compost were watered with tap water. The day before the experiments, plants in Levington were given Liquinure solution until the compost was completely saturated and the "oles in the bottom of the pots stoppered. Aerator blocks were pushed into the soil- * Present address: Atomic Energy Agricultural Research Station, Tando Jam, West Pakistan. Ill
2 112 A. Q. ANSARI AND D. J. F. BOWLING water complex and the roots were aerated overnight. Next morning the plants were detopped and a plastic tube pushed over the stump to act as a reservoir for the xylem exudate. Plants in John Innes were watered with tap water to bring the compost to field capacity just before detopping. The pots were left unstoppered and no forced aeration was provided. The electrical potential difference between the soil and the exuding sap was measured using a high impedence millivoltmeter and the following electrode system. Calomel electrode 3MKCL agar salt bridge Sap Root system Soil solution Calomel electrode Glass micropipettes with tip diameters of approximately ioo /im were used for holding the salt bridges to minimize contamination of the sap with KCl. Tbe experimental set-up is sbown diagrammatically in Fig. i. Electrometer Recorder Reference electrode Test electrode in xylem sap Soil Fig. I. Diagram of the experimental layout for measuring the electrical potential difference between the soil and the exuding sap of detopped sunflower plants grown in potting compost. Immediately after tbe potential was measured samples of tbe sap and soil solution were taken for analysis. The soil solution in the Levington compost was obtained by simply filtering soil samples. With the John Innes compost at field capacity samples were centrifuged at approximately 1000 g for 5 minutes and the supernatant filtered. K and Mg were determined by flame emission spectrophotometry, Ca and Mg hy atomic absorption spectrophotometry, NO 3 and Cl using specific ion electrodes (Orion), and SO4 by precipitation with BaClj; the precipitate estimated by nephelometer. ph of the soil water and exudate was also measured. The electrochemical potential difference (or the driving force) on an ion j distributed between the soil water and the xylem sap can be calculated as follows: Afij = zf{e,^, - Ej) J/g ion where z ionic valency, F = the Faraday, E^^,^ = the measured potential difference (i)
3 Trans-root electrical potential 113 (mv) between the sap and soil solution and Ej is the Nernst potential for the ion (mv). At room temperature Ej can be calculated from the following equation: for cations, or Ej = ^ logp] for anions, (2) where C^ and Cj are the concentrations (mm) of the ion in the soil water and the sap respectively. EXPERIMENTAL RESULTS There was good electrical continuity between the reference electrode in the wet compost and the test electrode in the exuding sap. In preliminary experiments the reference electrode was moved around the pot and the trans-root potential noted at each location. Results obtained from plants in both Levington and John Innes compost are shown in Table i. They show that the position of the reference electrode in the soil had a relatively Table i. Measurement of the electrical potential difference {mv) between the soil and the exuding sap of detopped sunflower roots with the reference electrode at different places in the soil Position of electrode in the soil I A B A, root in Levington compost saturated with water, 6 hours after detopping; B, root in John Innes compost at field capacity, 2 hours after detopping. small effect on the potential difference between the soil and the exuding sap. Nevertheless, all the values of potential difference reported below are means of five or six deteritiinations with the soil electrode at different locations in the pot to eliminate any possibility of error from this source. Ion concentrations in the soil water and the exuding sap and values of A/7 and f^bs for roots in Levington compost are shown in Table 2 and for plants in John Innes compost in Table 3. The Liquinure treatment appears from comparison of Tables 2 and 3 to have increased the concentration of K, NO, and Mg in the soil water of the Levington. The concentrations of the other ions studied are virtually the same in both composts. The concentrations of Mg, NO3 and K in the sap of the plants grown in Levington are also higher than those of the John Innes plants. Despite these differences the values of A/7, except for SO4, are qualitatively the same for both sets of plants. Positive values for cations and negative values for anions indicate transport into the xylem sap against the cltctrochemical potential gradient. The higher ionic concentrations in the Levington compost appear to have caused a feduction in the trans-root potential. This would be expected in the light of results obtained from plants grown in water culture. A tenfold increase in the concentration of the
4 A. Q. ANSARI AND D. J. F. BOWLING Table 2. Electrical potentials {E^^,^, ion concentrations in the soil water and the xylem sap and electrochemical potential differences {Afi) for sunflower plants grown in Levington compost 6 hours after they were detopped {data are means + standard error of mean of results from six plants) Concentration Concentration A/i Ion in sap (mm) in soil water (mm) kj/g ion K 23.9±i.4 g.6±o.4 -(-0.52 Na i.2±o ~3.6s Cl ii.4±i.2 5.5±i.i NO3 25.7±i.3 3i-5±i SO ~i.33 Mg 3.3±o Ca 7.3 ± ± ph 5.2±o.2 5.4±o.i 0.60 Potential (mv) E,b Table 3. Electrical potentials (Eobs). ion concentrations in the soil water and the xylem sap and electrochemical potential differences (A/I) for sunflower plants grown in John Innes compost 6 hours after detopping {data are means ± standard error of the mean of results from five plants) Ion K Na Cl NO3 SO4 Mg Ca ph Concentration in sap (mm) 8.9±i.7 i.7±o ± ±0.5 I.2± ±0.5 S-3±o.8 5.6±o.2 Concentration in soil water (mm) ± ±o ± ±o-2 kj/g ion O-53 Potential (mv) E,^, i \l Time after \^^ detopping (hours) I Fig. 2. The trend in the electrical potential of the xylem sap with respect to the soil; results irom two plants grown in Levington compost.
5 Trans-root electrical potential IO\t ^ Time after detopping (hours) ^^^ I Fig. 3. The trend in the electro-chemical potential gradient with time for CS, NO3 and SO4; data from a plant grown in Levington compost. #, SO4;, NO3; A, Cl. culture solution resulted in a fall of approximately i8 mv in tbe trans-root potential (Bowling, 1966). The trans-root potential difference was observed to change slowly from the time it was first determined after the plants were detopped. It became progressively less negative with time and after 24 hours it had usually changed from a negative to a positive value (Fig. 2). The concentrations of the ions in the sap, however, remained virtually unchanged over this period. Figs. 3 and 4 show the trend in A/I values of the various ions for a plant in Levington compost allowed to exude for 24 hours after detopping. The values for both anions and cations show a tendency to fall to zero and even to become positive. Fig. 4. Electrochemical potential gradients for several cations plotted against time; data from a plant, grown in Levington compost, allowed to exude for 24 hours after de-topping., K; o, Ca;, Mg; A, Na.
6 ii6 A. Q. ANSARI AND D. J. F. BOWLING DISCUSSION There are certain limitations which apply to the interpretation of the data for the electrochemical potential gradients reported above. In the case of cations a negative value for A// suggests that the ion is moving down the electrochemical potential gradient and that the root is not doing any work to move it from the soil into the xylem. However, it is possible that there is an active cation transport to the xylem which is masked by a large passive flux as has been suggested by Pitman and Saddler (1967) and Jennings (1967). Furthermore, absorption of cation by the tissues at the base of the stem would give rise to a spuriously low cation concentration in the exuded sap which could lead to a negative value for A/i even though the cation concerned is being actively transported across the root. This possibility was suggested by Briggs (1968). However, the work of Meiri and Anderson (1970) with excised corn roots indicates that there is no evidence, at least for potassium, of absorption from the xylem fluid by the surrounding tissues. Finally a negative value for A/I could be interpreted in terms of active cation transport from the xylem back towards the soil. For these reasons we can conclude very little about the behaviour of Ca, Na and Mg from the data in Tables 2 and 3 except that the large negative values for A/J suggest that these ions are moving passively into the xylem sap. Hydrogen ions appear to be very near to passive equilibrium suggesting that there is no proton pump in these roots. A positive A/I value for cations indicates transport against the electrochemical potential gradient. We can be fairly confident about this because it is difficult to explain how the cation concentration in the sap could be maintained at a higher level than that predicted on purely physical grounds in any other way than by postulating active transport. Whilst we cannot be certain of the significance of negative values for cations, negative driving forces on anions moving across the detopped root system are virtually certain to mean active transport. Where the trans-root potential is negative a flux of negative ions into the xylem sap can only be maintained by the expenditure of metabolic energy. We can see from Tables 2 and 3 that NO3 and Cl are being actively transported into the xylem sap by quite large driving forces. The behaviour of SO4 differed depending on the compost in which the plants were grown. In Levington compost it was apparently being pumped into the sap but in John Innes compost the SO4 concentration in the sap was much lower than in the sap of the plants grown in Levington, giving rise to a positive A/I value. However, the driving forces on SO^ for both sets of plants were very low suggesting that the influx pump for SO4 was very weak making it undetectable in the John Innes plants 6 hours after detopping. Salt uptake and transport by sunflower plants have been shown to be closely dependent on the supply of assimilates reaching the root via the phloem (Bowling, 1968). It is. therefore, not surprising to find a fall oflf in the driving forces moving the anions into the xylem after decapitation of the root (Fig. 3). The gradient down which Ca and Mg appeared to be moving declined with time after detopping until it was zero after 24 hours (Fig- 4)- ^^ is possible that this gradient is set up by the active transport of the anions as the driving forces on the anions and the gradient acting on Ca and Mg both declined at the same rate. The trends in the driving forces acting on K and Na are very interesting because immediately after detopping both ions appeared to be moving to the xylem down the electrochemical gradient, but 24 hours after detopping they were clearly being actively pumped mto the xylem sap because the trans-root potential was positive at that time
7 Trans-root electrical potential 117 (Fig. 2). In earlier work (Bowling, 1966; Bowling and Ansari, 1971) we obtained evidence that water culture grown sunflower roots are able to accumulate both potassium and sodium against the electrochemical potential gradient. In the freshly detopped exuding root it seems that this active transport is swamped by large passivefluxesof these cations presumably brought about by the large flux of anions. However, as the anion flux declines the passive cation flux also declines revealing the active cation transport. It is also interesting that this active cation flux continues long after tbe active anion flux and it suggests that the two types of transport are driven by different mechanisms. Mac- Robbie (1965) obtained evidence that K uptake in the alga Nitella translucens is supported by energy obtained by ATP bydrolysis but tbat Cl uptake is directly linked to electron transfer reactions and does not depend on phosphorylation. It is possible that similar systems for cation and anion uptake occur in roots. The results obtained with these soil grown plants are very similar to those obtained with plants grown in water culture (Bowling, 1966; Sobey et al., 1970) indicating that the presence of the soil, at least under the conditions of our experiments, did not markedly alter the processes of salt transport to the shoot. We believe that this approach for studying salt transport across the root, which started as a laboratory technique, has now been successfully extended to the potted plant in the greenhouse. We can see no reason why it should not be exploited further to become a valuable method for use in the field. ACKNOWLEDGMENTS This work forms part of a thesis submitted for the degree of Ph.D. of the University of Aberdeen by A. Q. Ansari who gratefully acknowledges the receipt of a Colombo Plan Fellowship. REFERENCES BOWLING, D. J. F. (1966). Active transport of ions across sunflower roots. Planta, 69, 377. BOWLING, D. J. F. (1968). Translocation at o" C in Heliaitthus annuus. J. e.xp. Bot., 19, 381. BOWLING, D. J. F. & ANSARI A. Q. (1971). Evidence for a sodium influx pump in sunflower roots. Planta, BOWLING, D. J. F. & SPANSWICK H. M. (1964).. \ctive transport of ions across the root oi Ricinus cotnmunis. y. Exp. Bot. 15, 422. BOWLING, D. J. F., MACKLON, A. E. S. & SPANSWICK, R. M. (1966)..Active and passive transport of the major nutrient ions across the root of Ricinus communis. J. exp. Bot., 17, 410. BRIGGS, G. E. (1968). Passive movement of water and solutes into the absorbing region of the root. J. p.v/i. Bot., 19, 486. JENNINGS, D. H. (1967). Electrical potential measurements, ion pumps and root exudation a comment and a model explaining cation selectivity by the root. Nezo Pliytol., 66, 357. "^IACROBBIE, E. A. C. (1965). The nature of the coupling between light energy and active ion transport in Nitella translucens. Biochim. biophys. Acta, 94, 64. "liri, A. &. ANDERSON, W. P. (1970). Observations on the e.xchange of salt between the xylem and neighbouring cells in Zea mays primary roots. Jf. e.\p. Bot., 21, 908. PITMAN, M. G. & SADDLER, H. D. \V. (1967). Active sodium and potassium transport in cells of barley roots. Proc. natn. Acad. Sei., U.S.A., 57, 44. SOBEY, D. G., MACLEOD, L. B. & FENSOM, D. S. (1970). The time course of ion and water transport across decapitated sunflowers for 32 hours after detopping. Can. J. Bot., 48, 1625.
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