Kinetics of Root Elongation of Maize in Response to

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Crop Science, 24, 1090-2. PRITCHARD, J., TOMOS, A. D., and WYN JONES, R. G., 1987. Control of wheat root elongation growth. I. Effects of ions on growth ...

Journal of Experimental Botany, Vol. 39, No. 208, pp. 1513-1522, November 1988

Kinetics of Root Elongation of Maize in Response to Short-Term Exposure to NaCl and Elevated Calcium Concentration1 Department of Land, Air and Water Resources, University of California, Davis, CA 95616, U.S.A. Received 21 June 1988

ABSTRACT Cramer, G. R., Epstein, E. and Lauchli, A. 1988. Kinetics of root elongation of maize in response to short-term exposure to NaCl and elevated calcium concentration.—J. exp. Bot. 39: 1513-1522. To study the effect of salt (NaCl) on root elongation we developed a device that measures this effect by means of a Linear Variable Differential Transformer (LVDT). To test the efficacy of the device we performed experiments demonstrating that (a) rates of elongation of primary maize (Zea mays L.) roots were comparable to elongation rates of primary roots growing freely in solution culture; and (b) chilling and low O 2 concentrations of the solution elicited the expected responses. Inhibition of root elongation by 75 mol m " 3 NaCl was gradual. At an iso-osmotic concentration, mannitol did not inhibit root growth, suggesting that the inhibition was not due to osmotic factors but rather to effects of salt on metabolism. The addition of supplemental Ca (10 mol m" 3 ) ameliorated this stressful condition. Timing of the application of Ca was critical. Treatment with Ca after addition of NaCl only partially restored growth, but pretreatment with Ca completely prevented the inhibition of growth by salt stress. Key words—Root growth, Zea mays L., salinity. Correspondence to: Department of Plant Science, University of Nevada, Reno, NV 89557, U.S.A.

INTRODUCTION Both the physiological and the cellular and molecular responses of plants to stress are of much interest (Mussell and Staples, 1979; Key and Kosuge, 1985). They may also afford clues for environmental management and genetic manipulation of plants so as to optimize their performance under stressful conditions. Schulze (1986) and Munns and Termaat (1986) have reviewed the important roles that roots seem to play in the regulation of shoot growth during exposure of plants to drought and salinity. Salt stress has both osmotic and physiological-biochemical-metabolic components (Munns and Termaat, 1986). Further, plant responses to salt stress are affected not just by the total salinity as measured by the osmotic potential or specific electrical conductance, but also by the specific chemical composition of the saline medium (Kingsbury and Epstein, 1986; Termaat and Munns, 1986). Specifically, much attention has been paid to the role of calcium 1

Supported by National Science Foundation grant DMB84-04442 to A.L. and E.E. Present address and to whom correspondence should be sent: Department of Plant Science, University of Nevada, Reno, NV 89557, VS.A. 2

@ Oxford University Press 1988

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Cramer et al.—Kinetics of Root Elongation

MATERIALS AND METHODS Design of apparatus

Early attempts to develop a device to measure root elongation involved choosing a design similar to that of Evans (1976), which required the root to press upon the device. This proved unsatisfactory, because theflexibleroots tended to bend in solution upon root extension rather than giving direct displacement downwards. We then chose a different approach, maintaining the root under slight tension, keeping it straight in solution, and directing displacement downwards. We have developed a device modelled on that used by Hsiao et al. (1970) to measure leaf elongation, with some modifications. The design of the root elongation device is shown in Fig. 1. Our device uses a Schaevitz 250-HPD LVDT (Linear Variable Differential Transformer). Two innovations are: (1) attachment of the line to the root and (2) adjustment of the LVDT core during the course of the experiment. A cap, cut from a 50 to 200 mm3 disposable pipette tip and tied to the line, was attached to the root cap with Duro Super Glue (Loctite Corporation, Cleveland, Ohio, U.S.A.). The cap had to be small enough to ensure that it did not extend beyond the region of the root cap or else subsequent root elongation would be inhibited as a result of direct bonding to the elongating region. In our case the cap was approximately 2-0 mm long. Attachment of the root to the line with the glue was successful. The glue could be applied to the root cap in very small quantities, gave a strong bond, and dried quickly (30 s were sufficient), thus minimizing the time during which the root was exposed to light and air. In addition, there was no toxic effect of the glue on the root (see Results and Discussion). Eventually the root cap would be sloughed off the root, disconnecting the line. We re-attached the line to the root several times over a period of 3 d without any apparent disturbance to the root. Lead weights (9-2 g total weight) were placed on the line to counterbalance the weight of the LVDT core (15 g) and to prevent excessive tension on the roots. Some weight (5-8 g) on the line was maintained in order to keep some tension to facilitate movement of the line through the pulleys. When the core reached the limits of the linear span of the LVDT, the core was readjusted by isolating it from the line leading to the root, using a stop on the pulley at the top of the apparatus. This stop consisted of a screw-down clamp with a rubber wedge shaped to fit in the groove of the pulley wheel.

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in counteracting to some extent the effect of salt (NaCl) on plant growth (Gerard, 1971; Hyder and Greenway, 1965; Kent and Lauchli, 1985; Kurth, Cramer, Lauchli, and Epstein, 1986; LaHaye and Epstein, 1969, 1971; Maas and Grieve, 1987; Norlyn and Epstein, 1984) and in affecting a number of other salt-related phenomena (Ayoub, 1974; Cramer and Lauchli, 1986; Cramer, Lauchli, and Polito, 1985; Imamul Huq and Larher, 1984; Wadleigh and Bower, 1950). To understand how an environmental stress affects plant growth, we mayfirstask what are the primary stress responses that, in time, are responsible for the observed effects on growth. In the present investigation we sought answers to the following questions. Upon salinization of the medium with NaCl (75 mol m " 3 ), is the observed diminution of maize root elongation due to osmotic or specific ion effects? What effect does calcium at elevated concentration (10 mol m~3) have on root elongation when the medium is salinized? To answer these questions we modified the design of a device for measuring shoot elongation (Hsiao, Acevedo, and Henderson, 1970) so that it could be used for measuring root elongation over time. Other devices have been developed to measure continuous leaf growth (Waldron, Terry, and Nemson, 1985) and roots (Evans, 1976; Kuzmanoff and Evans, 1981; Tanimoto and Watanabe, 1986). In this work, wefirsttested the efficacy of the device by measuring the responses of roots to low temperature and oxygen concentrations. We demonstrated that it adequately measures root elongation. We then showed that the primary roots of maize seedlings respond differently to salt stress. In particular, we demonstrated that the initial response of root elongation to salt stress is dependent upon the external Ca concentration. At a low Ca concentration, root elongation is inhibited by ionic rather than osmotic stress. At a high Ca concentration, root elongation is not impaired in the short term; there are neither ionic nor osmotic effects.

Cramer et al.—Kinetics of Root Elongation


Power Supply Chart Racortiar

FIG. 1. Diagram of the root elongation device. An expanded window in the top right corner depicts more clearly the stop device on the top pulley.

The clamp was screwed down holding the string tightly against the pulley. A spring was placed in the clamp to facilitate release of the rubber end from the pulley when the clamp was unscrewed. Once the root was isolated from the LVDT core, the string attached to the rod of the core could be readjusted. The string was attached to the rod by passing it through a small hole at its end. A small spring was fitted over the end of the rod connected to the LVDT core. This served to fasten the string securely to the end of the rod after it had passed through the small hole in the tip of the rod. The core was re-positioned by slipping the spring off the rod, pulling up the excess slack in the line that had accumulated from the movement of the core during root growth and refastening the spring over the line on the tip of the rod. This procedure facilitated repeated measurements of the growth of the root over the linear span of the LVDT without disturbing the root, which was very sensitive to vibrations and jolts (see Feldman, 1984, for physiological responses of roots induced by mechanical stress). The type of line used proved to be important. Initially we used a twisted nylon fishing line, but later found that this was sensitive to temperature fluctuations of as little as 1 °C resulting from random temperature and humidity cycles in our laboratory. Waxing the twisted line with melted parafilm reduced the line's response to temperature and humidity fluctuations. Monofilament fishing line and thin copper wire proved to be as sensitive to temperature and humidity as the twisted nylon line. We now use a line made of Kevlar (Dupont, Edmund Scientific, Barrington, New Jersey, U.S.A.) which has a negligible response to temperature and humidity fluctuations under our laboratory conditions. Growth conditions Maize seeds (Zea mays L. cv. Pioneer 3377) were germinated in 0 5 mol m~ 3 CaSO 4 at 27°C. After 3 d in the dark, the primary root of a seedling was connected to the line of the root elongation device and placed on a plastic grid at the surface of a 01 modified Hoagland solution (Epstein, 1972) in a 3-5 dm 3 polyethylene container. The nutrient solution was kept at 29 °C unless otherwise stated. Treatments were imposed when root growth had reached a steady rate. Details of each treatment are described in the respective figure legends.

RESULTS AND DISCUSSION In preliminary experiments we tested the device with young cotton seedlings. However, it was difficult to distinguish between elongation of the hypocotyl and the root. Furthermore, the rate of root elongation was only about 1-0 mm h" 1 and there was a long lag period (approximately 4 h) after handling of the root during which it did not elongate. In contrast,

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Cramer et al.—Kinetics of Root Elongation





FIG. 2. The effect of temperature on root elongation. The temperature was controlled with a Lauda K-2/RD Temperature Controller. Temperature was recorded with a temperature probe on a YSI Model 32 conductance meter. The growth rates of three different roots are presented here. The symbols for temperature correspond to the symbols of the respective root. The root represented by the square symbol (closed) disconnected itself from the LVDT at 5-2 h. One hour after reconnection, the growth rate of the root was equal to its previous rate before cooling (data not shown).

maize seedlings did not give rise to the complications of an elongating hypocotyl, they grew at a rate of about 2-2 + 07 mm h" 1 (the fast rate facilitated measurements of responses to environmental stresses) and had half the lag period after handling. As we became more adept with the techniques, we reduced this lag period to 0-5 min. The rates of elongation in our device were not significantly different from rates observed for roots growing freely in solution culture under the same environmental conditions (2-2 ±0-2 mm h~'). These rates are about 25% less than those found by Sharp, Silk, and Hsiao (1988). These researchers used low salt concentrations (01 mol m~3 CaSOJ in a vermiculite medium, whereas we used solution culture (01 modified Hoagland solution) for growing the roots, which may be responsible for the slower growth rate. Effects of temperature The effect of temperature on root elongation is shown in Fig. 2. Root elongation was very sensitive to temperature. Growth rates were maximal between 25 °C and 29 °C; growth ceased at temperatures between 8°C and 10 °C. As the temperature was further increased, growth did not resume until the temperature reached 27 °C or higher, approximately 1 to 2 h after the initial rise in temperature. Root elongation was rapid once growth resumed, returning to the original growth rate prevailing before cooling had begun. The temperature response described above was as expected for a manifestation of growth mediated by metabolism. There was no evidence that the root was simply being stretched.

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Cramer et al.—Kinetics of Root Elongation


The tension on the root did not appear to be excessive, because no elongation was observed when the temperature was between 8 °C and 10 °C. The inhibition of elongation between 8 °C and 10°C suggests that the response of maize roots to temperature is analogous to the general growth response of chilling-sensitive plants (Minorsky, 1985). Effects of near anoxia

Anaerobic conditions were difficult to impose in our open 3-5 dm3 containers, but by reducing the volume to 2-0 dm3 and covering the top of the container, we were able to lower the O 2 concentration to 1% by bubbling N2 gas through the solution. Root elongation was inhibited rapidly with reduction of O 2 concentration (Fig. 3). Jackson and Drew (1984) report that the threshold O 2 concentration at which root elongation begins to slow is about half that of air. Our findings are in agreement with this. Upon a rapid return to aerobic conditions, two of the four roots immediately resumed normal growth rates; the other two roots showed lag times of 1 h and 3-5 h, respectively, before reaching their previous growth rates. This shows that there is considerable individual variability in recovery to anaerobic stress, although the immediate response to the stress was fairly uniform. Unlike low temperatures, nearly anaerobic conditions never completely inhibited growth. In their review on the responses of plants to anaerobiosis, Jackson and Drew (1984) reported that maize roots were able to survive anaerobic conditions for up to 70 h. The inhibition of cell division in Viciafaba roots was reversible if the duration of anaerobic stress was less than 12 h; and anaerobic conditions restricted entry of cells into mitosis but did not inhibit those already dividing (Jackson and Drew, 1984). Furthermore, they point out that the O 2

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FIG. 3. The effect of anoxia on root elongation. Nearly anaerobic conditions were imposed by bubbling N 2 through the nutrient solution. The O 2 concentration was monitored with a YSI Model 53 oxygen monitor. Each symbol represents an individual root and its respective oxygen concentration in the nutrient solution.


Cramer et al.—Kinetics of Root Elongation



concentration at which root elongation ceases is difficult to predict because of the influence of the stirring rate on the unstirred layers at the root surface, the effectiveness with which air contamination of the medium is prevented, the extent to which O 2 diffuses from the shoot within the gas spaces of the root, and the radial leakage of O2 from the root to the medium. The lack of complete inhibition of root elongation could have been influenced by any one of the above factors (the roots were 4 to 6 cm long). Nevertheless, this experiment supports the conclusions drawn from the temperature experiment, that the experiments did indeed measure metabolic root elongation. Effects of salt stress The effects of salt stress on root elongation are shown in Fig. 4. When 75 mol m " 3 NaCl was added, there was an immediate but small inhibition of root growth. Growth continued to be progressively inhibited over the next 4 to 5 h. Roots treated with an iso-osmotic concentration of mannitol (Fig. 5) also showed an immediate but small decline in growth rate (statistically insignificant), but returned to normal rates within an hour. There was some


Tlnw(h) FIG. 5. The effect of 138 mol m 3 mannitol (iso-osmotic with 75 mol m 3 NaCl) on root elongation. Mannitol was added at the time indicated by the arrow. The data represent the mean of three replicates. PLSD of the growth rate = 1-46.

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FIG. 4. The effect of salinity on root elongation over time. NaCl (75 mol m 3) was added at the time indicated by the arrow. The data represent the mean of three replicates. PLSD of the growth rate = 093.

Cramer et al.—Kinetics of Root Elongation



FIG. 6. The effect of salinity (75 mol m 3) on root elongation followed by treatment with supplementary Ca (10 mol m " 3 ). NaCl and CaCI 2 were added at the times indicated by the arrows. The data represent the mean of five replicates. PLSD of the growth rate = 0635.

Thiel, Lynch, and Lauchli (1988) found that leaf elongation of barley was affected by addition of both salt and mannitol to the root medium. There was an immediate inhibition of growth followed by a gradual recovery to a new steady rate which was proportional to the lowered water potential. After recovery, approximately 1 h after initiation of the treatment, roots treated with mannitol had a greater rate of leaf elongation than those treated with salt. Thus the response of barley leaf elongation to salt and water stress appears to differ from the response of maize root elongation, although, as in our study, there were differences in plant response to salt and water stress. Supplementary calcium had significant effects on the elongation of salt-stressed roots of maize. When supplementary Ca (10 mol m~ 3 final concentration) was added after the imposition of salt stress (Fig. 6), the growth rate gradually increased over the next 6 h, but never reached the original level prevailing before addition of NaCl during the course of the experiments. If, however, the supplementary Ca was added before the addition of NaCl, root elongation was not inhibited at all upon the addition of NaCl (Fig. 7). These results provide further evidence that Ca in the external solution can ameliorate the

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variability in the immediate response to addition of osmoticum, some roots being affected and others unaffected by the sudden imposition of osmoticum. The results of the mannitol experiment contrast with those of Sharp et al. (1988) who found that elongation of primary maize roots was inhibited by decreasing water potentials in the range of our experiments. Westgate and Boyer (1985), however, found that elongation of nodal maize roots was not inhibited by decreasing water potentials in this range. Other researchers (Kuzmanoff and Evans, 1981; Taylor and Ratliff, 1969), using different plant species, did not observe significant inhibition of primary root elongation in the range of water potentials used in this study. The water potentials of a 01 modified Hoagland solution and a 75 mol m~ 3 NaCl solution are approximately equal to 00074 and 0-34 MPa, respectively. Perhaps the use of low salt-grown roots in the study by Sharp et al. (1988) decreased the ability of those roots to adjust osmotically to lower water potentials, or influence wall extensibility properties. With regard to salt stress, Pritchard, Tomos, and Wyn Jones (1987) attributed the inhibition of root elongation by 10 mol m " 3 K to ionic effects on wall extensibility rather than turgor.


Cramer et al.—Kinetics of Root Elongation 3.0






3.0 Tlmo(h)




FIG. 7. The effect of salinity (75 molm 3) following pre-treatment with supplementary Ca( 10 mol m~ 3 ). CaCl 2 and NaCl were added at the times indicated by the arrows. The data represent the mean of 13 replicates. PLSD of the growth rate = 0645.

inhibition of root growth by NaCl. In earlier studies (Cramer, Lauchli, and Epstein, 1986; Kurth et al, 1986) it was shown that the inhibition of growth of cotton roots by NaCl stress could be completely mitigated by 10 mol m~3 Ca. High Ca concentrations maintained cell length and rates of cell production in cotton roots exposed to salinity (Kurth et al, 1986). It would appear that maize roots respond in a similar way to those of cotton. In earlier, long-term experiments with bean plants, Ca at 10 mol m~3 completely reversed the inhibitory effect of 50 mol m " 3 NaCl on growth (LaHaye and Epstein, 1969, 1971). All these findings from experiments done with several species, over both short and long periods, show good agreement. The gradual response to NaCl with 0-4 mol m" 3 Ca suggests the onset of an internal metabolic dysfunction and that this is a more important factor in the growth response than changes in physical events related to the immediate reduction in the water potential (i.e. turgor). This conclusion is supported by the fact that neither the iso-osmotic mannitol treatment nor the high Ca/NaCl treatment inhibited growth significantly over the time-course of our experiments. These results do not imply that the immediate displacement of membrane-associated Ca (Cramer et al, 1985) by Na is unimportant as a primary response to salinity, because this response could lead to ion toxicity or nutrient imbalance through changes in membrane permeability and selectivity which, in turn, could cause a metabolic inhibition of root elongation. This reasoning is supported by the following: (1) addition of supplementary Ca could not completely restore growth once the salt stress had already been imposed and (2) it was vital for continued normal root growth rates that high Ca concentrations be present in the nutrient solution before the addition of NaCl. In summary, we have shown that root elongation was completely inhibited by cool temperatures between 8°C and 10°C, but was only partially inhibited by low O 2 concentrations. Salt stress (75 mol m" 3 NaCl) slowed the rate of root elongation. High Ca levels in the external nutrient solution completely protected the root from salt stress if present before the stress was imposed, despite the fact that CaCl2 at 10 mol m~3 substantially decreased the osmotic potential of the solution. Ourfindingsthus confirm the importance of the ionic composition of the medium with regard to the responses of plants to salt stress and, specifically, the role of calcium in modulating these responses.

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Cramer et al.—Kinetics of Root Elongation


HSIAO, T. C , ACEVEDO, E., and HENDERSON, D. W., 1970. Maize leaf elongation: continuous

measurements and close dependence on plant water status. Science, 168, 590-1. HYDER, S. Z., and GREENWAY, H., 1965. Effects of C a + + on plant sensitivity to high NaCI concentrations. Plant and Soil, 23, 258-60. IMAMUL HUQ, S. M., and LARHER, F., 1984. Osmoregulation in higher plants: effect of maintaining a constant Na: Ca ratio on the growth, ion balance and organic solute status of NaCl-stressed cowpea (Vigna sinensis L.). Zeitschrift fur Pflanzenphysiologie, 113, 163-76. JACKSON, M. B., and DREW, M. C , 1984. Effects of flooding on growth and metabolism of herbaceous plants. In Flooding and plant growth. Ed. T. T. Kozlowski. Academic Press, New York. Pp. 47-128. KENT, L. M., and LAUCHLI, A., 1985. Germination and seedling growth of cotton: salinity-calcium interactions. Plant, Cell and Environment, 8, 155-9. KEY, J. L., and KOSUGE, T. (Eds), 1985. Cellular and molecular biology of plant stress. Alan R. Liss, New York. KINGSBURY, R. W., and EPSTEIN, E., 1986. Salt sensitivity in wheat. A case for specific ion toxicity. Plant Physiology, 80, 651-4. KURTH, E., CRAMER, G. R., LAUCHLI, A., and EPSTEIN, E., 1986. Effects of NaCI and CaCl 2 on cell

enlargement and cell production in cotton roots. Ibid. 82, 1102-6. KUZMANOFF, K. M., and EVANS, M. L., 1981. Kinetics of adaptation to osmotic stress in lentil (Lens culinaris Med.) roots. Ibid. 68, 244-7. LAHAYE, P. A., and EPSTEIN, E., 1969. Salt toleration by plants: enhancement with calcium. Science, 166, 395-6. 1971. Calcium and salt toleration by bean plants. Physiologia plantarum, 25, 213-18. MAAS, E. V., and GRIEVE, C. M., 1987. Sodium-induced calcium deficiency in salt-stressed corn. Plant, Cell and Environment, 10, 559-64. MINORSKY, P. V., 1985. An heuristic hypothesis of chilling injury in plants: a role for calcium as the primary physiological transducer of injury. Ibid. 8, 75-94. MUNNS, R., and TERMAAT, A., 1986. Whole-plant responses to salinity. Australian Journal of Plant Physiology, 13, 143-60. MUSSELL, H., and STAPLES, R. C. (Eds), 1979. Stress physiology in crop plants. John Wiley and Sons, New York. NORLYN, J. D., and EPSTEIN, E., 1984. Variability in salt tolerance of four triticale lines at germination and emergence. Crop Science, 24, 1090-2. PRITCHARD, J., TOMOS, A. D., and WYN JONES, R. G., 1987. Control of wheat root elongation growth. I. Effects of ions on growth rate, wall rheology and cell water relations. Journal of Experimental Botany, 38, 948-59. SCHULZE, E.-D., 1986. Whole-plant responses to drought. Australian Journal of Plant Physiology, 13, 127-41. SHARP, R. E., SILK, W. K., and HSIAO, T. C , 1988. Growth of the maize primary root at low water potentials. I. Spatial distribution of expansive growth. Plant Physiology, 87, 50-7. TANIMOTO, E., and WATANABE, J., 1986. Automated recording of lettuce root elongation as affected by auxin and acid pH in a new rhizometer with minimum mechanical contact to roots. Plant and Cell Physiology, 27, 1475-87.

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LITERATURE CITED AYOUB, A. T., 1974. Effect of calcium on sodium salinization of beans {Phaseolus vulgaris L.). Journal of Experimental Botany, 25, 245-52. CRAMER, G. R., and LAUCHLI, A., 1986. Ion activities in solution in relation to Na + -Ca 2 + interactions at the plasmalemma. Ibid. 37, 321-30. and EPSTEIN, E., 1986. Effects of NaCI and CaCI2 on ion activities in complex nutrient solutions and root growth of cotton. Plant Physiology, 81, 792-7. -and POUTO, V. S., 1985. Displacement of Ca 2 + by Na + from the plasmalemma of root cells. A primary response to salt stress? Ibid. 79, 207-11. EPSTEIN, E., 1972. Mineral nutrition of plants: principles and perspectives. John Wiley and Sons, New York. Pp. 39. EVANS, M. L., 1976. A new sensitive root auxanometer. Preliminary studies of the interaction of auxin and acid pH in the regulation of intact root elongation. Plant Physiology, 58, 599-601. FELDMAN, L. J., 1984. Regulation of root development. Annual Review of Plant Physiology, 35, 223-42. GERARD, C. J., 1971. Influence of osmotic potential, temperature, and calcium on growth of plant roots. Agronomy Journal, 63, 555-8.


Cramer et al.—Kinetics of Root Elongation

TAYLOR, H. M., and RATLIFF, L. F., 1969. Root elongation rates of cotton and peanut as a function of soil strength and soil water content. Soil Science, 108, 113-19. TERMAAT, A., and MUNNS, R., 1986. Use of concentrated macronutrient solutions to separate osmotic from NaQ-specific effects on plant growth. Australian Journal of Plant Physiology, 13, 509-22. THIEL, G., LYNCH, J., and LAUCHLI, A., 1988. Short-term effects of salinity stress on the turgor and elongation of growing barley leaves. Journal of Plant Physiology, 132, 38-44. • WADLEIGH, C. H., and BOWER, C. A., 1950. The influence of calcium ion activity in water cultures on the intake of cations by bean plants. Plant Physiology, 25, 1-12. WALDRON, L. J., TERRY, N., and NEMSON, J. A., 1985. Diurnal cycles of leaf extension in unsalinized and salinized Beta vulgaris. Plant, Cell and Environment, 8, 207-11. WESTGATE, M. E., and BOYER, J. S., 1985. Osmotic adjustment and the inhibition of leaf, root, stem and silk growth at low water potentials in maize. Planta, 164, 540-9. Downloaded from at Site Universitaire de Bordeaux on June 11, 2015

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