Agronomy Journal 92:868-874 (2000)
© 2000 American Society of Agronomy
ROOT DEVELOPMENT
Growth and Potential Conductivity of White Clover Roots in Dry Soil with Increasing Phosphorus Supply and Defoliation Frequency
Dhananjay K. Singha and
Peter W.G. Saleb
a CSIRO Plant Industry, Frank Wise Institute, P.O. Box 19, Kununurra, Western Australia 6743 and Dep. of Agricultural Sci., La Trobe Univ., Bundoora, Victoria 3083, Australia
b Dep. of Agricultural Sci., La Trobe Univ., Bundoora, Victoria 3083, Australia
dsingh{at}agric.wa.gov.au
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ABSTRACT
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Shallow-rooted white clover can be exposed to severe water stress during dry periods, leading to poor growth and persistence in pastures. Root growth is a primary determinant of drought tolerance and water uptake in dry soils, which may interact with P supply and defoliation frequency for grazed white clover in legume-based pastures. Effects of four levels of P supply (0, 17, 50, and 150 mg P kg-1 soil), two defoliation frequencies (frequent and infrequent), and two soil water regimes (wet and dry) were determined on various parameters associated with root growth and plant water uptake. A microscopy study was also undertaken to measure the relative size and abundance of xylem vessels in the primary roots of frequently defoliated low (P0) and high P (P150) plants. Increased P supply increased the rate of water loss per pot, which was better related to the coarse root length density compared with the fine root length density in dry soil. Coarse root length density, leaf area, mean number and diameter of xylem vessels, and potential root hydraulic conductance increased 6.2-, 12.4-, 2.4-, 1.5-, and 12.7-fold, respectively, for the frequently defoliated plants in dry soil between P0 and P150 treatments. It also appeared that leaf area and rate of water loss were dependent on the mean xylem diameter and associated hydraulic conductance. Increased P supply improved the ability of frequently defoliated white clover plants to tolerate dry soil conditions by lowering the resistance to water flow in roots and increasing the water uptake.
Abbreviations: Kh, hydraulic conductance, 
m, soil matric water potential • 
g, gravimetric water content
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INTRODUCTION
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WHITE CLOVER (Trifolium repens L.) is an important component of legume-based Australian dairy pastures, which can be exposed to drought from time to time even in the higher rainfall regions. Although the susceptibility of shallow-rooted white clover to drought is widely accepted (Hart, 1987; Turner, 1990), Singh et al. (1997) reported how increased P nutrition for white clover improved soil-plant water relations. High-P plants maintained greater leaf water potential in dry soil without showing moisture stress symptoms and extracted more soil water than P-deficient plants, which wilted rapidly in the drying soil and failed to recover on rewatering. These moisture stress symptoms were more severe if the low-P plants were frequently defoliated. In that experiment, clover plants were exposed to different defoliation frequencies to simulate variations in grazing pressure, as restrictions in forage supply during dry periods can result in more frequent grazing by livestock.
Evidence in the literature suggests that the drought tolerance of tea, onion, and cotton is increased by improved root growth and root functioning in response to increased P supply (Nagarajah and Ratnasuriya, 1978; Nelsen and Safir, 1982; Radin and Eidenbock, 1984). O'Toole and Chang (1979) found drought-resistant rice varieties to have longer roots that were thicker in diameter than those of susceptible varieties. They concluded that these roots supplied essential water during drought. An increase in root diameter, however, suggests a larger stele with more xylem vessels in high-P roots compared with low-P roots. Any change in the diameter of a xylem vessel has a profound effect on the potential conductivity of that vessel, given that the hydraulic conductance of a narrow vessel is proportional to the fourth power of the vessel diameter for ideal capillaries (Hagen-Poiseuilles law) (Calkin et al., 1986). Accordingly, Hargrave et al. (1994) and Cruz et al. (1992) pointed out that wider xylem vessels, with their minor resistance to water flow, should contribute much more to the overall hydraulic conductance of the xylem tissues than narrow vessels.
Our objective was to examine whether increased root growth and changes in xylem diameter and density of primary roots can explain the beneficial effects of high P levels on white clover tolerance to dry soil conditions. We hypothesized that increased soil P concentration would not only increase the total root growth in dry soil, it would also improve the water uptake by lowering the resistance to water flow in basal primary roots as a result of increased mean xylem diameter and density, compared with low-P plants.
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Materials and methods
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Experimental Design and Treatments
The experiment was a randomized complete block design with four replicates on benches in a temperature-controlled glasshouse with natural light and an air temperature regime of 25°C (±5°C) in Melbourne, Australia (37°20' S, 145°02' E). Air relative humidity varied between 30 and 80% during the experimental period. A total of 64 cylindrical PVC tubes (0.33 m long and 0.16 m wide), closed at one end, were filled with 5.5 kg each of an air-dried, well-mixed, low-P (Olsen 5 mg kg-1) clay-loam Krasnozem soil (Gn4.11, Northcote, 1974) (Eutrustox, U.S. classification). The pots had been cut longitudinally in two halves and then taped together to enable easy recovery of roots to be measured at the end of the experiment.
Treatments included the factorial combination of four P rates (0, 17, 50, and 150 mg P kg-1 oven-dried soil, designated as P0, P17, P50, and P150), two defoliation frequencies (plants defoliated every 14 and 28 d across a 56-d experimental period for the frequent and infrequent defoliation treatments, respectively), and two soil water regimes (a wet and a dry treatment). For the wet treatment, the soil matric water potential (m) in the bulk soil was maintained gravimetrically (kg kg-1, gravimetric water content [g]) between -0.01 and -0.03 MPa, which corresponded to 0.430 and 0.367 g. The m for the dry treatment was maintained between -0.04 (0.355 g) and -1.5 MPa (0.305 g). The relationship between m and g had been determined using a pressure plate previously (Singh et al., 1997). Since high-P plants had not shown any water stress symptoms at -1.5 MPa m previously, m in the dry regime was cycled between -0.04 and -1.5 MPa (Singh et al., 1997).
Growing Conditions
Two stolons with two to three leaves and nodal roots were selected from mini-swards of white clover (cv. Kopu) that had been established from the same clonal material. The rooted stolons were planted in the pots after the roots were immersed in a concentrated Rhizobium legunminosarum biovar trifolii slurry, and grown for 10 wk with regular watering before the onset of the experiment. The P treatments were applied by thoroughly mixing appropriate amounts of Ca(H2PO4)2·H2O in powder form with 7.3 mg N [Ca(NO3)·4H2O], 18.2 mg K (K2SO4), 7.3 mg Ca (CaCO3), 14.6 mg S (elemental S), 0.7 mg Mn (MnSO4·H2O), 0.7 mg Zn (ZnSO4·7H2O), 0.7 mg B (Na2B4O7·H2O), 0.3 mg Cu (CuSO4·5H20), and 0.05 mg Mo [(NH4)6Mo7O24·4H2O] kg-1 air-dried soil as basal nutrients. The soil surfaces were covered with 30 mm of polystyrene beads (4 mm in diameter) to minimize water evaporation. The required amount of water for the respective water treatments was determined gravimetrically, by weighing the pots, and applied on daily basis.
Anatomical Studies
Anatomical studies were undertaken only for the frequently defoliated P0 and P150 plants subjected to wet or dry conditions. At final harvest on Day 56, basal portions of 20 mm length from two main primary roots per pot were sampled and fixed in 4% glutaraldehyde with 0.025 M phosphate buffer (O'Brien and McCully, 1981). Root segments were dehydrated in ethanol and embedded in white resin after 10 d of fixation in a series of white resin concentrations. Polymerization was done overnight at 70°C in bean gelatine. Embedded root segments were then cut in ultrathin sections of 8 to 10 µm on a sliding microtome. Sections were immediately stained with toluidine blue and fast green, with subsequent drying under vacuum suction and heat, and mounted in Eukitt (Carlzeiss Prop. Ltd., Melbourne, Australia) for examination. Transverse sections of stele and cortex area were examined at a magnification of 200x, and the diameter and number of xylem vessels were measured and counted.
For electron microscopy, 2- to 3-mm transverse and 5- to 10-mm longitudinal sections were removed from gluteraldehyde-fixed root portions with a sharp twin-sided blade. These freehand-cut sections were dehydrated in ethanol, dried with liquid CO2, and coated with Au–Pd. Longitudinal and transverse gold-plated root sections were examined at 300 to 4500x with an auto-scan electron microscope at 15 kV, and photographed.
Measurements
Root Parameters and Root–Shoot Ratio
At the final harvest on Day 56, all fully expanded leaf blades plus their petioles and stolons were harvested, and leaf area was measured with a leaf area meter (Delta-T Devices, Burwell, Cambridge, UK). Roots were carefully removed from the soil core, washed, and recovered on a 0.5-mm mesh. Roots with a diameter >1 mm were defined as coarse roots and were separated from fine roots. Roots were dried for 3 h at room air temperature, and the remaining water was then blotted from the roots with paper towels before determining root fresh mass for both size classes. To determine total root length according to Tennant (1975), coarse and fine roots were then spread out on a 5-mm grid. Root length density was calculated as root length (m) per kg air-dried soil. Mean root diameter (d) was determined using the formula [(root fresh mass/root length) x 
]1/2 of Schenk and Barber (1979). Leaf, stolon, and root dry masses and root (coarse + fine root mass) to shoot (leaves + stolons mass) ratio were measured after drying all plant material at 70°C in an oven for 48 h.
Rate of Water Loss
The rate of water uptake by clover plants exposed to the different treatments during a 52-d period was determined by gravimetrically measuring the rate of water loss during the final 4 d of the experimental period (Day 53 to Day 56). On Day 53, all plants were watered to bring their m to the upper limit according to the wet and dry treatments. For example, plants subjected to the dry treatment were watered to bring their m to -0.04 MPa. Similarly, plants exposed to the wet treatment were watered to -0.01 MPa. During these 4 d, pots were weighed every morning and evening, but water was applied to the wet treatment only when required to maintain the m between -0.01 and -0.03 MPa. No additional water was given to the plants exposed to dry treatment, though the m in some of the infrequently defoliated P50 and P150 plants fell below the -1.5 MPa on the third day. It is important to note that between Day 1 and Day 52, all plants were maintained according to the wet and dry soil water regimes.
The rate of water loss per hour from the pots was calculated as the rate of total water loss per pot. Surface water evaporation through the polystyrene bead layer was accounted for by subtracting the water loss from a control pot with surface beads but no plants. Beads were able to reduce soil water evaporation by 100% for the dry soil treatment and by 98% for the wet soil treatment.
Potential Root Hydraulic Conductance (Hagen-Poiseuille Prediction for Kh)
The potential root hydraulic conductance (Kh) was calculated from xylem diameters using the Hagen-Poiseuille equation (Gibson et al., 1984; Woodhouse and Nobel, 1982) as follows:
where d is the diameter in m of the ith vessel, n is the total number of xylem vessels, and 
is the viscosity of water in MPa s (dynamic viscosity of water at 20°C is 
10 Pa s; Milburn, 1979). However, the presented Kh is based on the mean xylem vessel diameter and mean number of vessels.
Statistical Analysis
Analyses of variance were performed to test effects of the main treatments, P supply, defoliation frequency, and soil water regime and their interactions. Separate analyses of variance were also performed for the frequent defoliation treatment, as the frequently defoliated low-P plants were particularly sensitive to dry soil conditions (Singh et al., 1997; Singh and Sale, 1998). Regression analyses were performed to examine the relationships between rate of water loss, and coarse and fine length densities and leaf area.
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Results
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Frequently defoliated low-P plants (P0 and P17) growing under drought stress displayed similar water stress symptoms, such as wilting of leaves with some stolon mortality by the end of the fourth defoliation cycle, as observed in a previous experiment (Singh et al., 1997). No such symptoms occurred in high-P plants (P50 and P150). Relative shoot yield, leaf P concentration, stolon density, leaf number, and leaf area increased for frequently and infrequently defoliated plants in wet and dry soil with increasing P supply (Singh and Sale, 1998).
Fine Roots
Compared with the unfertilized control, the mass and root length density of fine roots increased about 3.6-fold with P application at a rate of 150 mg kg-1 soil (Table 1)
. Increased defoliation frequency resulted in a 40% decrease in the mass and root length density of fine roots. The soil water regime did not have any effect on the growth of fine roots, and there were no interactions between soil water regime, P supply, and defoliation frequency treatments for the measured root parameters.
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Table 1 Analysis of variance and main effect treatment means for P supply, defoliation frequency (cycles over 56 d), and soil water regime ( m, MPa), for coarse and fine root mass and root length density
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Coarse Roots
Increased P supply markedly improved the mass and root length density of coarse roots, and there was a three-way interaction between P supply, defoliation frequency, and soil water regime (Table 1). Coarse root growth varied in response to P supply depending on defoliation regime for the wet and dry soil water regimes. For example, root length density for the infrequently defoliated (Fig. 1a)
and frequently defoliated plants (Fig. 1b) was significantly greater in the wet soil than in the dry soil for all P treatments except for P50 (infreqent defoliation) and P150 (frequent defoliation). These P levels were apparently able to reduce the detrimental effect of drought stress on the growth of coarse roots in this study. Similar responses and interactions were also observed for the root mass (data not presented).
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Fig. 1 Effect of increasing P supply on the coarse root length density for (a) infrequently and (b) frequently defoliated white clover plants in wet (solid circles) and dry (open circles) soil. Error bars represent ± one standard error of the mean
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Mean coarse root diameter also increased with increasing P supply. However, the response to added P depended on P supply and soil water regime. The interaction primarily resulted from a twofold increase in mean coarse root diameter, from 0.10 mm to 0.20 mm, for the dry treatment, compared with only a 42% increase, from 0.12 mm to 0.17 mm, for the wet treatment, when P supply increased from 0 to 150 mg kg-1 soil.
Rate of Water Loss
The total water uptake by the roots and its transport to the shoots was affected by P supply. Water loss per pot increased threefold from 1.2 to 3.8 g h-1 between P0 and P150 (Table 2)
. Increased defoliation frequency, on the other hand, reduced the rate of water loss per pot by 40% (Table 2). Compared with wet soil, the dry soil treatment reduced the total water loss per pot by 30%.
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Table 2 Analysis of variance and main effect treatment means for P supply, defoliation frequency (cycles over 56 d), and soil water regime (m, MPa), for the rate of water loss, leaf area, and root/shoot ratio on a dry mass basis
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When the water loss data for frequently defoliated plants were analyzed separately, there were significant interactions between P supply and soil water treatments (Fig. 2)
. The rate of total water loss per pot was lower in the dry soil at low levels of added P, but was equal to that of the wet soil at the highest P rate.
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Fig. 2 Effect of increasing P supply on rate of total water loss for frequently defoliated white clover plants in wet (solid circles) and dry (open circles) soil. Error bars represent ± one standard error of the mean
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Influence of Leaf Area and Root–Shoot Ratio on Water Loss
Similar to coarse root mass, leaf area was affected by a three-way interaction between P supply, defoliation frequency, and soil water regime. This interaction translated to a more than 12-fold increase in the leaf area (from 23 to 282 cm2) of frequently defoliated plants in the dry soil, compared with only a three-fold increase in the wet soil (from 68 to 207 cm2) between P0 and P150 treatments.
Root–shoot ratio declined (P < 0.001) with increasing P supply by 35% between the P0 and P150 treatments (Table 2). However, it increased significantly (P < 0.05) with increased defoliation frequency, whereas dry soil water regime had no significant effect on the root–shoot ratio (P > 0.05). There was no interaction between treatments for the root–shoot ratio, and the data indicate that the root–shoot ratio had no effect on the rate of water loss.
Relationship between Rate of Water Loss and Coarse Root
A positive linear relationship was found between the rate of water loss per pot and the fine and coarse root mass (Fig. 3)
. However, the relationship between the water loss in the dry soil and coarse root growth was much closer
than with fine roots
. The equivalent correlation coefficients between rate of water loss and root growth in the wet soil were 0.63 and 0.55 for coarse and fine roots respectively, showing much weaker relationships for the wet soil compared with the dry soil.
Phosphorus Supply and Anatomical Changes in Frequent Defoliated Plants
Increased P supply affected all anatomical features observed in this study when P supply increased from 0 to 150 mg kg-1 soil (Table 3)
. The ratio of stele to cortex area of frequently defoliated plants increased by 14% in wet soil and 89% in dry soil. Similarly, greater responses in mean number and diameter of xylem vessels occurred with increased P supply under dry compared with wet soil treatment (P < 0.05) (Table 3).
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Table 3 Analysis of variance and main effect treatment means for P supply (mg kg-1 soil) and soil water regime (m, MPa) for primary root diameter, average area of cortex and stele, ratio of stele to cortex area, total number of xylem vessels, and mean xylem diameter in the primary roots for frequently defoliated white clover plants
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Low-P roots in wet soil had a similar number of xylem vessels but 20% larger mean xylem diameter compared with dry conditions. In contrast to low-P plants, high-P plants had about 14% more xylem vessels with a 9.4% larger mean xylem diameter under dry compared with wet conditions. Also, the cell wall of the xylem vessels in primary roots appeared to be more distinct and dense for high-P than low-P plants (Fig. 6A and 6B)
.
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Fig. 6 Transverse sections of xylem tissue of (A) P0 and (B) P150 photographed at 1700x magnification, and longitudinal sections of the P0 photographed at (C) 950x and (D) 2200x. The P0 treatment (A) had thinner xylem walls (comparable walls are identified by arrows), with some of the conduits blocked by starchlike granules (S), compared with the thicker xylem walls of the P150 treatment (B), which lacked starchlike granules. (C) shows the abundance of starchlike granules in most of the P0 conduits. (D) shows the presence of mucilage and bacterial growth (BG) in one of the vessel elements of the P0 treatment
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Potential Root Hydraulic Conductance
Phosphorus supply had a very marked impact on the mean potential hydraulic conductance (Kh) of primary roots. The potential conductance, estimated from the mean diameter and mean number of xylem vessels in primary roots, increased 3.7- and 12.5-fold for wet and dry treatments, respectively, between P0 and P150 treatments (Fig. 4) .
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Fig. 4 Effect of P supply and soil water treatments on the potential hydraulic conductance (Kh), estimated from mean number of xylem vessels and diameter in primary roots of frequently defoliated white clover plants
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It should be noted that increasing the P supply from 0 to 150 mg kg-1 soil resulted in an almost similar magnitude of increases in Kh and leaf area for wet and dry conditions. For example, leaf area, like Kh, increased around three- and 12-fold between P0 and P150 for wet and dry conditions, respectively. There was also a highly significant (P < 0.001) positive linear relationship between Kh and the leaf area of frequently defoliated plants (Fig. 5a)
. Similarly, there was a close but curvilinear relationship
between Kh and the rate of water loss per pot (Fig. 5b).
Foreign Materials in Low-Phosphorus Conduits
The conduits of the low-P roots also contained an abundance of foreign materials that appeared like starchlike granules, mucilage, and/or bacterial growth (Fig. 6A, 6C, and 6D). Starchlike granules were observed in the central stele portions inside the tracheids (Fig. 6A), whereas mucilage and/or bacterial growth was detected inside the xylem vessel elements (Fig. 6D). The suspected blockage of conduits with foreign material would further reduce the conductive capacity of the xylem vascular system inside the primary roots of low-P plants, compared with high-P roots, which had no foreign materials visible inside their conduits (Fig. 6B).
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Discussion
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The close relationship between the rate of water loss and coarse root length density in dry soil was a key finding. Increased coarse roots in association with fine roots, and overall increased root length density in response to increasing P supply, would result in greater extraction of soil water from a drying soil. Although Dodd et al. (1992) reported an increased dry matter partitioning to white clover roots growing in dry soil, they did not differentiate this partitioning between coarse and fine roots. The present study, however, provides some evidence for a greater dry matter partitioning to coarse roots in dry soil with increasing P supply compared with wet soil. High P levels reduced the detrimental effect of drought stress on the coarse root length density of frequently or infrequently defoliated plants and enabled these plants to extract adequate water from the drying soil for their maintained growth and survival, particularly for the frequently defoliated plants (Fig. 1 and 2).
Increased P supply had a profound effect on potential hydraulic conductance of the primary roots. The relevant increase in the diameter of basal root (Table 3) was not unexpected because of the increased size of these plants; the high-P plants had greater shoot and root masses and total leaf areas compared with the P0 plants (Singh and Sale, 1997; Singh and Sale, 1998). Surprisingly, roots of similar diameter were significantly different in stele area and ratio of stele to cortex in response to soil water or P supply. The increase in the total number of xylem vessels for the high-P roots appeared to be associated with an approximate twofold increase in the ratio of stele to cortex (Table 3), which would provide more area for the development of xylem vessels. Increased mean xylem diameter resulted in a large increase in the potential root hydraulic conductance for the high-P plants in dry soil (Fig. 4). However, the rate of water loss per pot increased in a curvilinear way with increasing Kh (Fig. 5b). This was probably due to a lower availability of water in the drier soil for the high-P plants. Nevertheless, results indicated that high-P clover plants certainly were less likely to have conductivity constraints in meeting the increased transpirational demand from their larger leaf area. Therefore, it should not be surprising that high-P plants were able to better tolerate the dry soil conditions than low-P plants (Singh et al., 1997).
The parallel increases in the leaf area and potential root hydraulic conductance between low- and high-P clover plants under wet or dry conditions (Fig. 5a) is consistent with the findings of Radin and Eidenbock (1984), who reported parallel decreases in leaf area and hydraulic conductance in low- and high-P cotton plants. They also noted that differences in hydraulic conductance due to low-P supply clearly preceded any effects on leaf area development, and concluded that hydraulic conductance limited the leaf expansion by restricting water transport.
The resistance to water flow in roots of low-P plants would increase further if xylem vessels became blocked, as observed in this study (Fig. 6). There were a number of primary xylem vessels in the low-P clover roots that contained mucilage and/or bacterial growth in the lumen of the vessel, indicating that these vessels were dead. North and Nobel (1992) reported the presence of mucilage in the secondary xylem of roots of Opuntia ficus-indica (L.) Mill. in dry soil. Some of the conduits of low-P clover roots appeared to be blocked by the presence of starch granulelike particles (Fig. 6). Starch accumulation has been reported in dicotyledonous roots of white clover (Soper, 1959). A reduced conductive capacity of the low-P clover roots due to the resistance to water flow would contribute to a lower tolerance of dry soil conditions as observed previously (Singh et al., 1997).
In conclusion, increased drought tolerance of frequently defoliated high-P clover plants was apparently related to their greater root growth, particularly coarse root length density, and increased mean xylem diameter in the primary roots. Consequently, an increased root conductivity of these plants enhanced the water uptake and leaf area expansion, even under dry conditions, compared with low-P plants.
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ACKNOWLEDGMENTS
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The authors acknowledge the financial support provided by Pivot Agriculture (Australia) for this research. The work forms a part of a larger research program, Phosphorus for Dairy Farm, that is based at the Ellinbank Dairy Research Institute, Dep. of Natural Resources and Environment, Ellinbank, Victoria, Australia. We are also grateful to Denise Fernando for her assistance with the electron microscopy.
Received for publication December 18, 1998.
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ABSTRACT
INTRODUCTION
