Journal of Experimental Botany, Vol. 36, No. 170, pp. 1441-1456, September 1985

Root Growth and Water Uptake by Maize Plants in Drying Soil R. E. SHARP 1 AND W. J. DAVIES 2 Department of Biological Sciences, University of Lancaster, Bailrigg, Lancaster LAI 4YQ, U.K. Received 12 February 1985

The influence of soil drying on maize (Zea mays L.) root distribution and use of soil water was examined using plants growing in the greenhouse in soil columns. The roots of plants which were watered well throughout the 18 d experimental period penetrated the soil profile to a depth of 60 cm while the greatest percentage of total root length was between 20-40 cm. High soil water depletion rates corresponded with these high root densities. Withholding water greatly restricted root proliferation in the upper part of the profile, but resulted in deeper penetration and higher soil water depletion rates at depth, compared with the well watered columns. The deep roots of the unwatered plants exhibited very high soil water depletion rates per unit root length. Key words—Maize, roots, water deficit, soil water depletion. Correspondence to. Department of Biological Sciences, University of Lancaster, Bailrigg, Lancaster LAI 4YQ, U.K.

INTRODUCTION During the last 20 years there has been considerable controversy over the effects of soil drying on the magnitude of the various resistances to water transport in the pathway between the soil some distance away from the root and the root xylem. There is now some consensus that even at relatively high bulk soil water potentials, substantial localized hydraulic resistances may develop both in the soil immediately adjacent to the roots (perirhizal resistance) (Caldwell, 1976) and, where there is inadequate contact between the soil and the root surfaces at the soil: root interface (Herkelrath, Miller, and Gardner, 1977a, b; Faiz and Weatherley, 1977; 1978). The latter may result from soil or root contraction (Huck, Klepper, and Taylor, 1970) and because roots frequently grow down channels in the soil (Taylor, 1974) or from the activity of soil fauna (Atkinson and Wilson, 1979). A high resistance to water flow at the soil: root interface over an appreciable part of the total root surface would, in addition, enhance the development of perirhizal resistance around the remainder of the root system. Caldwell (1976) has emphasized that continued root extension within the region of the soil profile in which the plant already has a well-established root system is of advantage in evading such localized high resistances. Extensive root proliferation within the rooted zone 1

Present address: Department of Land, Air and Water Resources, University of California, Davis, California 95616, U.S.A. 2 To whom correspondence should be addressed.

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ABSTRACT Sharp, R. E and Da vies, W. J. 1985. Root growth and water uptake by maize plants in drying soil.— J. exp. Bot. 36: 1441-1456.

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Sharp and Davies—Root Growth and Water Uptake by Maize Plants

will, however, result in rapid soil water depletion. Because of the resistance to water movement through the soil to the root zone (pararhizal resistance) (Newman, 1969), prohibitively low bulk soil water potentials may develop, and plant water uptake will become dependent on continual root proliferation into unexplored regions of the soil profile. Only a small part of the total root system may then be involved in water absorption, and the quantity of water taken up by the plant may be closely related to the length of root present per unit volume of soil in which water is available (Russell, 1977). Thus, in drying soil, species or varieties that exhibit extensive and deeply penetrating root systems can more thoroughly exploit the available soil water, and are in general comparatively drought tolerant (Hurd, 1974; Burch and Johns, 1978; Burch, Smith, and Mason, 1978; Garwood and Sinclair, 1979). It should be noted, however, that if water is not available at depth and plants are dependent on stored water near the soil surface, a less extensive root system may be advantageous (Passioura, 1981). In addition, the advantage to the plant of an extensive root system must be weighed against the cost of growing and maintaining roots. The optimum root growth for a crop plant and a wild plant may, therefore, be rather different (Passioura, 1981).

MATERIALS AND METHODS Seeds of Zea mays L. cv. John Innes Fl hybrid were germinated in seed trays containing a 1:1 mix of peat and sand. At the seed leaf stage, 80 plants were selected for uniformity and each planted in a vertical soil column (10 cm diameter and 80 cm depth) contained in a 10m length of polythene tubing. The columns were supported by a three tier wire mesh frame which was surrounded by black polythene to prevent light from reaching the roots. Each tube was tied at the base, and perforated at the base and at 10 cm intervals of depth to allow free drainage and aeration of the soil. The tubes werefilledwith sieved John Innes No. 2 potting compost (approximately 6-3 kg oven dry weight per tube). A single mix of soil was used for the experiment. After initialfilling,the soil was watered well and allowed to settle. More soil was then added and the tubes rewatered; this process was repeated to give afinalsoil depth of 80 cm. Seven extra soil columns were prepared for determination of the mean bulk density and the water content at field capacity of the soil in each 10 cm layer. The experiment was conducted in a greenhouse with day and night air temperatures of 25-30 °C and around 20 °C, respectively. Humidity was uncontrolled. The plants received 16 h days (light period

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In 1875, Muller-Thurgau concluded that relatively dry soil conditions induced plants to develop a more extensive root system. This generalization has been affirmed by numerous reports that the development of soil water deficits can increase both lateral root proliferation (for example, Weaver, 1926; Kmoch, Ramig, Fox, and Koehler, 1957; Sharma and Ghildyal, 1977; Osonubi and Davies, 1978; Huck, Ishimara, Peterson, and Ushijima, 1983) and the depth to which roots penetrate the soil profile (for example, Bennett and Doss, 1960; Allen, 1977; Sharma and Ghildyal, 1977; Malik, Dhankar, and Turner, 1979; Molyneux and Davies, 1983). Such morphological changes in the root system may result in increases in total root length (Sharma and Ghildyal, 1977; Osonubi and Davies, 1978) and total root dry weight (Bennett and Doss, 1960; Malik et al., 1979) when compared with well watered plants. It seems likely that these root growth 'responses' increase the effectiveness of the root system in the exploitation of soil water, although comparisons of the water extraction characteristics of well watered and unwatered plants have not been reported. In an earlier study (Sharp and Davies, 1979), we reported that potted maize seedlings subjected to mild soil water deficits exhibited a substantial absolute increase in root growth, manifest in both the total length and dry weight of the root system. We suggested that these responses were, to some extent, a function of the high capacity for solute accumulation and turgor maintenance that was observed in root apices at low soil water potentials. In this report the influence of an extended period of soil drying on root distribution and soil water exploitation was examined using seedlings growing in soil columns to allow relatively unrestricted root development.

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RESULTS The plants, which were watered well throughout the experimental period, exhibited a marked day to day variation in mid-day leaf water potential which is a function of variation in ambient conditions in the greenhouse (Fig. la). Despite this, parallel changes in osmotic potential allowed the maintenance of a fairly constant level of leaf turgor. A similar but more pronounced variation in mid-day leaf water potential was recorded in the plants subjected to the 18 d soil drying treatment (Fig. lb). When compared with the well watered plants, a decrease in leaf water potential of approximately 0-35 MPa was already apparent by the second day after withholding water, although a substantially greater decrease was not recorded until after day 15. Corresponding decreases in osmotic potential maintained substantial leaf turgor throughout the experimental period, albeit at a lower level than in the well watered plants. These water relations measurements were intended as an indication of bulk shoot water status, and may not represent those of the expanding leaf cells (Michelena and Boyer, 1982). A marked reduction in mid-day leaf conductance (the combined diffusive conductances of both leaf surfaces) was apparent by the second day after withholding water (Fig. 2). This was followed by a progressively greater reduction, when compared with control values, during

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05.00 h to 21.00 h), natural sunlight being supplemented by two 250 W sodium lamps and two 250 W metal halide lamps (Thorn Lighting Ltd., London, England) to give a minimum photon flux density at plant height of approximately 200 ^mol m " 2 s " l (PAR). The plants were grown in the soil columns for 2 weeks prior to the start of the experiment. During this period all tubes were watered daily to run-off. At the start of the experiment, all tubes were watered at 22.00 h (day 0) and were allowed to drain to field capacity. The surface of the soil in each tube was covered with a polythene disc to reduce evaporation. Forty plants were chosen randomly as controls, and were watered at 22.00 h daily. The remaining plants were not rewatered for the 18 d experimental period. On alternate days to day 6, and then every 3 d, 5 tubes of both treatments were removed from the frame at 22.00 h (before the control plants were rewatered), and the plants were destructively harvested for measurements of leaf area and leaf, stem and ear dry weights. The soil columns were sectioned into 10 cm lengths and immediately subsampled in duplicate for the determination of soil water content as a percentage of oven dry weight (80 °C, 24 h). Bulk soil water (matric) potentials in the range —01 to — 1-5 MPa were calculated from a curve of soil water content against water potential constructed for the soil mix using a pressure plate apparatus. Soil water potentials below —1-5 MPa were not determined. The bulk of the roots were recovered from the soil by hand, and the total length and total dry weight of the roots recovered from each soil layer were determined. Root lengths were measured using an instrument modified from the design of Rowse and Phillips (1974). On the same days as plants were harvested, hygrometric measurements of mid-day leaf water and osmotic potentials were made from 60 mm diameter discs excised from the lamina of the youngest exposed leaf of five plants from each treatment. Leaf hygrometer design is described by Sharp (1981). Measurements were also made of the adaxial and abaxial diffusive conductances of recently expanded leaves using a Delta T Devices Mk II diffusion porometer. Five tubes were used for determination of the soil water content at field capacity. After watering, the tubes were tied to prevent evaporation from the soil surface, and were allowed to drain for 24 h. The mean water content of each 10 cm soil layer was then determined. To calculate the mean bulk density of the soil in each layer, two soil columns were sectioned into 10 cm lengths and weighed after oven drying at 80 °C for 48 h. The volume of each soil layer was 765 cm 3 . (Soil mean bulk density: 0 to 10 cm, 114 g cm" 3 ; 10 to 20 cm, 114 g cm" 3 ; 20 to 30 cm, 115 g cm" 3 ; 30 to 40 cm, 119 g cm" 3 ; 40 to 50 cm, 118 g cm" 3 ; 50 to 60 cm, 1-25 g cm" 3 ; 60 to 70 cm, 1-24 g cm" 3 .) Volumetric soil water contents were calculated by multiplying the soil water contents as a percentage of oven dry weight by soil bulk density, assuming that the density of water is 10 g cm" 3 . Soil water depletion rates from each 10 cm layer were calculated from the changes in soil water content between successive sampling days. Rates for well watered columns were calculated from the changes in soil water content from field capacity.

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Sharp and Davies—Root Growth and Water Uptake by Maize Plants

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the remainder of the experimental period, resulting in almost complete stomatal closure during the middle of the light period on the final day of the soil drying treatment. A limitation of shoot growth, manifest as a slower rate of leaf area (Fig. 3) and leaf dry weight development (data not shown), was already evident by the fourth day after withholding water. Nevertheless, both leaf and stem growth were maintained, although at progressively more reduced rates when compared with the control plants, throughout the soil drying treatment. At the end of the experiment, the leaf area and leaf and stem dry weights of the unwatered plants were 60-70% of the control values. Despite the marked limitation of shoot vegetative growth, the soil drying treatment caused only a slight retardation of ear development (data not shown). The rate of increase in total root dry weight was not slowed until after the sixth day of the soil drying treatment (Fig. 4). In contrast to the results of earlier studies (Sharp and Davies, 1979), there was no evidence of an absolute increase in root dry weight during the development of water deficits. At the beginning of the experiment, the bulk of the root system was distributed within the upper 20 cm of soil, although a few roots had reached the 30-40 cm layer. As the experiment progressed, the roots of the well watered plants grew deeper into the soil profile, and by day 18 had penetrated to a depth of over 60 cm (Fig. 5). These plants developed a very dense root system in the upper soil layers, so that by the end of the experiment approximately 95 % of

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Sharp and Davies—Root Growth and Water Uptake by Maize Plants

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FIG. 2. The combined mid-day adaxial and abaxial diffusive conductances of the youngest expanded leaves of plants watered daily (•—•) and of plants not watered after day 0 (•—a). Points are means of at least six determinations + standard error.

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FIG. 3. The change in leaf area of plants watered daily (#—•) and of plants not watered after day 0 (o—o). Points are means of five measurements + standard error.

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Sharp and Davies—Root Growth and Water Uptake by Maize Plants 20-

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FIG. 4. The change in total root dry weight of plants watered daily (•—•) and of plants not watered after day 0 (o—o). Points are means of five measurements + standard error.

both the total root length and the total root dry weight was distributed within the upper 50 cm of soil (Fig. 6). Figure 6, showing root development as a percentage of the whole, is a useful illustration of where the roots are in the soil but is somewhat misleading since soil drying has not only caused a redistribution of root development with roots penetrating more deeply into the soil (Figs 5 and 6) but greatly restricted total root growth. This is illustrated for all soil layers in Fig. 5. It is noteworthy, however, that despite a cessation of root extension the root dry weight in the upper layers continued to increase, albeit at a lower rate than in the well watered tubes. For example, although there was no apparent increase in the total length of roots in the 0-10 cm soil layer after the second day of soil drying, an approximately threefold increase in root dry weight was recorded between days 2 and 18 (Fig. 7). This can, to some extent, be accounted for by the continued production of thick, unbranched nodal root axes which was observed throughout the soil drying treatment despite the development of very low soil water potentials around the base of the stem (Fig. 6). These roots would have made a substantial contribution to the total dry weight but not to the total length of roots in the upper soil layers. Vertical root growth was unimpeded by the development of plant water deficits, and after day 12 the root length density below 60 cm was substantially higher than the control value (Fig. 5). Furthermore, by day 18 a considerable root proliferation was apparent at a depth of

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FIG. 5. The change in mean root length density in consecutive 10 cm soil layers of tubes watered daily (•—•) and of tubes not watered after day 0 (o—o). Points are means of five determinations + standard error, (a) 0 to 10 cm, (b) 10 to 20 cm, (c) 20 to 30 cm, (d) 30 to 40 cm, (e) 40 to 50 cm, (f) 50 to 60 cm, (g) 60 to 70 cm, (h) 70 +cm.

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FIG. 6. The percentage of total root length and of total root dry weight in consecutive 10 cm soil layers after an 18 d period during which plants were either watered daily (open bars) or not watered after day 0 (shaded bars). Values are means of five determinations + standard error. The mean soil water content and approximate bulk soil water potential of each layer are indicated. W.S., water stressed. F.C, field capacity.

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Sharp and Davies—Root Growth and Water Uptake by Maize Plants

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DISCUSSION In a previous study (Sharp and Davies, 1979), we have demonstrated that nodal root apices of maize can adjust osmotically and maintain high turgor at low soil water potentials. We suggested that this turgor maintenance accounted for continued root extension in drying soil and, thereby, contributed to the enhanced root dry weights and lengths exhibited by plants growing in drying soil compared to those growing at high soil water potentials. It seems likely that a proportion of the solutes accumulating in roots under these conditions is current photosynthate which is made available for partitioning to the roots because of a decrease in shoot growth accompanied by only partial stomatal closure and the maintenance of a substantial rate of CO2 assimilation. A similar combination of events has been described by Shone, Whipps, and Flood (1983) for barley plants exposed to osmotic stress. In the present study, we have investigated the influence of soil drying on the dynamics of root development and water uptake by maize plants grown in containers where increased root growth may result in enhanced water availability. In contrast to our earlier study, unwatered plants grown in this system showed no enhancement of total root dry weight (Fig. 4) and shoot growth was sustained for the whole of the period of soil drying (Fig. 3). In this study, the effect of soil drying on root growth was to change the root distribution profile (Fig. 6). Intensive root proliferation in each soil layer ceased when the bulk soil water status fell below approximately 015 cm3 water cm" 3 soil or —005 MPa (compare Figs 5 and 8a), but roots continued to grow into deeper soil and eventually penetrated to a greater depth than those of well watered plants. The rate of water depletion from each layer decreased substantially in concurrence with the cessation of root proliferation (Fig. 8a). Therefore, the roots within soil layers at water potentials above approximately —05 MPa were considerably more effective in supplying water to the shoot than were the roots in drier soil. If an 'effective' root is thus defined as a root in a soil layer that had a mean bulk water potential greater than —0-5 MPa, then the total root length per plant that was 'effective' in supplying water at

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over 70 cm (Fig. 5). Thus, the roots of plants subjected to the soil drying treatment grew deeper into the soil profile than those of the well watered plants. The pattern of soil water depletion from unwatered tubes is shown in Figs 8a and b. These show, respectively, the change in the mean water content of successive 10 cm soil layers with time, and the soil water content profile at intervals during the soil drying treatment. Both the rate of soil water depletion (Fig. 8a) and the rate of root proliferation (compare Fig. 5) decreased substantially when the mean water content in each soil layer fell below approximately 0-15 cm3 water cm" 3 soil, corresponding to a bulk soil water potential of around —0-5 MPa. Thus, the zone of maximum water depletion shifted down the profile in dynamic correspondence with the progressive root proliferation into deeper soil layers, so that between days 15 and 18 the highest rate of soil water depletion was from below a depth of 60 cm. This point is more clearly illustrated in Fig. 9. The highest rate of soil water depletion from well watered tubes during thefinaldays of the experiment was recorded in the 20-30 cm layer, correlating with the highest root density, whereas soil water depletion rates at depths below 50 cm were considerably lower than from the unwatered tubes (Fig. 9). The data in Fig. 9 suggest that the few deep roots of the unwatered plants exhibit a very high rate of water uptake per unit root length when compared with control values, although it should be noted that vertical water flux towards the soil surface in response to a gradient of decreasing soil water potential will also have made some contribution to the observed pattern of soil water depletion.

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days

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FIG. 8. (a) The change in the mean water content of consecutive 10 cm soil layers of tubes not watered after day 0. (a) 0 to 10 cm (o), (b) 10 to 20 cm (•), (c) 20 to 30 cm (•), (d) 30 to 40 cm (•), (e) 40 to 50 cm (A), (f) 50 to 60 cm (A), (g) 60 to 70 cm (O)- Points are means offivedeterminations ± standard error, (b) The soil water content profile at intervals during the soil drying treatment; day 0 (•), day 2 (o), day 4 (•), day 6 (D), day 9 (•), day 12 (A), day 15 (A), day 18 (O)- Points are means of five determinations; standard errors are not shown (see Fig. 8a).

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Sharp and Davies—Root Growth and Water Uptake by Maize Plants a)

Or 10

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0 0 1 . .002 003 004 005 Soil water depletion rate (cm 3 cm"3 day"1)

006

FIG. 9. The mean soil water depletion rate from consecutive 10 cm soil layers of tubes watered daily (•—•) and of tubes not watered after day 0 (o—o) during (a) day 15 (well watered) and days 13 to 15 (unwatered), and (b) day 18 (well watered) and days 16 to 18 (unwatered). The numbers against the points are the mean root length densities (cm cm" 3 ) in each soil layer on day 15 (a) and day 18 (b).

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intervals during the soil drying treatment can be estimated. A similar analysis was reported by Klepper, Taylor, Huck, and Fiscus (1973). Table 1 shows that the rate of root proliferation into unexplored regions of the soil profile was sufficient to maintain a relatively constant (with the exception of the value recorded on day 12) 'effective' root length throughout the soil drying treatment. In addition, reference to Figs 8 and 9 suggests that, compared to roots of well watered plants, the few roots of the unwatered plants deep in the profile were extremely effective at removing water from moist soil. Comparable soil water depletion rates of between 0-03 and 0-04 cm 3 cm" 3 d~ 1 were shown by the two groups of plants even though the root length density of the unwatered plants in the zone where these rates were recorded was an order of magnitude lower than that of the well watered plants. An increased effectiveness of roots deep in the profile when upper soil layers have dried has also been noted by other workers (Taylor and Klepper, 1973; Stone, Teare, Mickell, and Mayaki, 1976; Gregory, McGowan, and Biscoe, 1978; Willatt and Taylor, 1978). 1. 'Effective' root length per plant (see text) of maize seedlings rooted in soil which remained unwatered after day 0. (Means of 5 +standard error)

TABLE

1236 + 54 cm 1741+42 cm 1413 + 213 cm 1281+273 cm 2028 + 149 cm 1446 + 244 cm

The overall result of this combination of changes in rooting characteristics was the maintenance of a substantial rate of water uptake and, thereby, the development of what were, arguably, only moderate leaf water deficits (Fig. 1), even after water had been withheld from the soil for 15 d. Stomata closed partially to restrict water loss, but CO 2 uptake by the unwatered plants must still have been substantial since both shoot (Fig. 3) and root (Fig. 4) growth continued throughout the soil drying treatment. The development of more severe water deficits at the end of the experiment, despite the highly effective exploitation of water deep in the profile, may perhaps have been attributable to a substantial axial resistance to water flow within the xylem of single primary root axes. Passioura (1972,1974) has suggested that when grasses, which can have only limited root xylem development, are extracting water mainly from deep in the subsoil, this resistance can result in large axial gradients in water potential between shoot and soil (see also Wilson, Hyder, and Briske, 1976; Molyneux and Davies, 1983). In species with only one seminal root axis, such as maize, the axial resistance of the root system may be particularly high if the surface soil is dry enough to prevent the growth of nodal axes (Passioura, 1981). In the present study, we observed that nodal axes continued to grow, albeit slowly, despite very substantial drying of the surface soil, presumably as a result of their high capacity for osmotic adjustment and turgor maintenance under these conditions (Sharp and Davies, 1979). It seems likely that the successful penetration of even a few nodal axes through dry upper soil layers and into moist soil deeper in the profile may be of considerable advantage. It is interesting to speculate on the mechanism which promoted the deeper penetration and more extensive proliferation at depth exhibited by the roots of the unwatered plants. Certainly, the rate of soil water depletion from depths below 50 cm was substantially higher in unwatered than in well watered tubes during the final days of the experiment (Fig. 9) and,

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Day 0 Day 2 Day 4 Day 6 Day 12 Day 18

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Sharp and Davies—Root Growth and Water Uptake by Maize Plants

When plants are dependent on water extracted from deep in the subsoil, it is clear that there would be a tendency for water loss from root to soil during upward water transport through dry surface soil layers. It is of major importance that this water loss should be minimized, both to conserve the available water and to prevent desiccation of the phloem and, thereby, to allow the continued growth and ultimately the survival of roots deeper in the profile. Thus, roots exposed to prolonged and severe soil drying may exhibit a pronounced suberization of the endodermis (McWilliam and Kramer, 1968; Shone and Flood, 1983), and the remnants of the plasmodesmatal channels through the endodermis may become blocked with callose or some other structural carbohydrate material (Clarkson and Robards, 1975). Deposition of suberized material has also been observed in the epidermis and hypodermis (Drew, 1979; Vermeer and McCully, 1982). These responses may have contributed to the substantial increase in dry weight per unit length of root which was apparent in the upper soil layers during the drying treatment (Fig. 8). Such conditions often result in the death of the root cortexes, and may largely prevent water and nutrient uptake by these roots following rewetting of the topsoil (Clarkson, Sanderson, and Russell, 1968; Passioura, 1981). It is important to note, however, that the roots of some plants may exhibit 'rectifier-like' activity and decreases in hydraulic conductance may be rapidly reversed upon rewatering (Nobel and Sanderson, 1984). This paper has emphasized the substantial redistribution of root growth of maize which can occur during soil drying, resulting in appreciable soil water depletion rates deep in the profile. However, substantial drying at depth increases the importance of water uptake from the topsoil following moderate rainfalls. We have previously noted that nodal root axes of maize have the capacity to osmotically adjust and continue slow growth even though the surface soil is very dry. Following rewetting, young nodal axes are ideally placed to ensure rapid resumption of water and nutrient uptake from the topsoil. Shone and Flood (1983) have recently emphasized the adaptive significance of this response in barley. ACKNOWLEDGEMENT R. E. Sharp thanks the S.E.R.C. for the award of a research studentship.

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therefore, these rooting characteristics may constitute important adaptive responses which increase the availability of soil water. It is important to note, however, the possibility that root growth at depth within the well watered tubes may have been restricted as a result of reduced aeration during the periods of near-saturation immediately following watering. It has been suggested that at soil moisture levels that approach saturation, even intermittently, aeration may exert a major influence on root development (Pearson, 1966). A similar argument could be forwarded to explain the deeper rooting exhibited by plants growing in drying soil in a number of previous studies (see Introduction). Nevertheless, a clear demonstration that the development of soil water deficits can induce deeper rooting was provided by Malik et al. (1979). Cotton seedlings were grown in soil at a range of water contents, and the growth of the roots into nutrient solution below the soil core was examined. Roots emerged from the soil cores earlier and exhibited a higher rate of elongation after emergence the lower the soil water content. It is noteworthy that abscisic acid, which is produced in large quantities in plants suffering water deficits, can also stimulate the growth of primary root axes (Yamaguchi and Street, 1977) and, thereby, increase the depth to which roots penetrate the soil profile (Watts, Rodriguez, Evans, and Davies, 1981). Abscisic acid may also increase the partitioning of carbohydrates to roots (Karmoker and Van Steveninck, 1979), and it is tempting to hypothesize that this mechanism is responsible for increased root growth in drying soil.

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LITERATURE CITED

ISHIMARA, K., PETERSON, C. M., and USHIJIMA, T., 1983. Soybean adaptation to water stress and

selected stages of growth. Ibid. 73, 422-7. HURD, E. A., 1974. Phenotype and drought tolerance in wheat. Agricultural Meteorology, 14, 39-55. KARMOKER, J. L., and VAN STEVENINCK, R. F. M., 1979. The effect of abscisic acid on sugar levels in seedlings of Phaseolus vulgaris L, cv. Redland Pioneer. Planta, 146, 25-30. KLEPPER, B., TAYLOR, H. M., HUCK, M. G., and Fiscus, E. L., 1973. Water relations and growth

of cotton in drying soil. Agronomy Journal, 65, 307-10. KMOCH, H. G., RAMIG, R. E., FOX, R. L., and KOEHLER, F. E., 1957. Root development of winter

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