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Inst. of Plant Sci., Group of Agron. and Plant Breeding, Swiss Federal Inst. of Technol. (ETH), Universitätstrasse 2, CH-8092 Zürich, Switzerland
* Corresponding author (walter.richner{at}ipw.agrl.ethz.ch)
Received for publication January 5, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Abbreviations: BD, soil bulk density • BDtop, topsoil bulk density • CT, conventional tillage • LA, leaf area • NT, no-tillage • Pc, phosphorus concentration in the shoot dry mass • PFUE, P fertilizer utilization efficiency • Ptop, P concentration in the topsoil • RLtop, proportion of total root length observed in the topsoil • SDM, shoot dry mass • Temptop, temperature of the topsoil • %Ntop, relative contribution of N uptake from the upper root zone to the total shoot N content
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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The objectives of this work were to study the combined effects of depth gradients of soil temperature, soil strength, and level of soil P on the early growth of maize under controlled conditions and, thus, to simulate soil physical conditions in the field under CT and NT. Emphasis was put on the growth, morphology, distribution, and functioning of the roots with regard to shoot growth and fertilizer utilization efficiency. Phosphorus was used as a model macroelement to determine whether the effects of soil properties on roots lead to an inadequate supply of nutrients to the shoot because the acquisition of P was found to be closely related to root growth (Mackay and Barber, 1984) and root morphology (Schenk and Barber, 1980).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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The growth columns were divided into two sections: an upper section, 10 cm long, and a lower section, 40 cm long. The upper section was closed at the lower end by a 3-mm steel wire mesh, which ensured unrestricted root growth, and the lower section was sealed at the bottom by a PVC disc. Each column section was filled with the growth substrate; the top 2 mm of the lower section were left free of substrate to prevent a vertical exchange of nutrient solution and to minimize heat transfer between the two sections. Subsequently, the two sections were fit together, and the connecting gap between the column walls was sealed with silicon caulk. After sowing one seed per column, the tops of the columns were capped to prevent evaporation from the soil surface and to minimize heat exchange with the air. The cap consisted of a watertight cylindrical container encasing a central PVC tube, to enable shoot growth, and four syringe needles (35 mm long) inserted downwards to ensure irrigation of the upper soil layer. The bottom of the cap was insulated with Styrofoam covered by aluminum foil. As the roots explored the lower section of the tubes later and to a smaller extent than the upper section, the lower section was not watered after the start of the experiment. Matric potentials of the substrate, which were determined using its water retention curve (Klute, 1986) and volumetric water contents measured at the last plant harvest, indicated that no water stress occurred with this watering regime. The lowest matric potentials at the end of the observed period of seedling growth were -30 kPa in the topsoil and -9 kPa in the subsoil.
The growth substrate was quartz sand (particle size of 0.08–0.2 mm) mixed dry with 5% (w/w) vermiculite powder (particle size of 0.08–0.1 mm) (Vermex Pulver E, Vermica AG, Bözen, Switzerland). This substrate was chosen because vermiculite has a good water- and nutrient-holding capacity (volumetric water content of 34.5% at a matric potential of -10 kPa, according to Lemaire, 1989; cation exchange capacity of 90–100 cmol kg-1; information provided by the supplier) and sand can be reproducibly packed, which is essential in root studies. Furthermore, sand is not cohesive; thus, its resistance to penetration varies little over a wide range of water contents in contrast to most soils, in which penetrometer resistance increases, often quite sharply, with decreasing soil water content (Tsegaye et al., 1995). To obtain a uniform volumetric water content of 20% in tubes of all treatments, independent of the dry soil bulk density (BD), 0.271 L of a modified Hoagland nutrient solution containing 7 mM of calcium nitrate [Ca(NO3)2], 2.0 mM of magnesium sulfate (MgSO4), 1.0 or 10.0 mM of phosphoric acid (H3PO4) (depending on the P treatment; see below), 1.5 mM of potassium sulfate (K2SO4), 0.16 mM of FeNA-EDTA, 0.05 mM of potassium chloride (KCl), 18.0 µM of manganese sulfate (MnSO4), 12.0 µM of boric acid (H3BO3), 1.5 µM of zinc sulfate (ZnSO4), 0.6 µM of copper sulfate (CuSO4), and 4.2 µM of molybdenum sesquioxide (MoO3) was mixed with the dry substrate of each tube. To get a nearly neutral pH, 1 mL L-1 sulfuric acid (H2SO4) was added to the nutrient solution. Nitrogen in the upper section (0–10 cm) was labeled with 10% 15N-enriched calcium nitrate (10.6 atom% 15N) (Isotec, Miamisburg, OH) so that the contribution of N taken up from this section to the total N content of the plant tops could be determined.
Experimental Treatments
The temperatures of the root zone were selected to coincide with typical soil temperatures from mid-April to early June in the Swiss Midlands. Three temperature levels [15 and 11, 17 and 13, and 19 and 15°C (day and night)] were applied to the topsoil while a uniform temperature was applied to the subsoil (15.5°C). The differences among the three temperature treatments were based on typical differences in topsoil temperatures between CT and NT systems. Under field conditions, daily fluctuations in temperature are much smaller at greater soil depths compared with the topsoil; thus, the temperature of the lower soil compartment was kept constant.
To induce soil mechanical resistance to root penetration, moist substrate was packed in the upper section of the tubes at three average BDs (1.15, 1.30, and 1.45 Mg m-3). The BD of the substrate in the lower section of the tube was 1.30 Mg m-3. Thus, bilayered columns consisting of either a layer with low BD on top of a layer with a higher BD or vice versa and homogeneously packed columns were obtained. Substrate in the bottom sections was packed, using a wood pestle, in 10-cm increments to achieve homogeneous BD over the whole depth. After each addition of substrate, the surface was scratched before more substrate was added to prevent the formation of a smeared layer. The choice of BD and moisture content levels represented a compromise: The chosen range of penetration resistance should be sufficient to impede but not completely halt root elongation, and the water content of the substrate should be sufficient for rapid root elongation while maintaining sufficient porosity. The resulting initial air-filled porosity was, depending on the BD treatments, between 20 and 27%; this is well in excess of the 10% aeration assumed to be acceptable for root growth and respiration (Grable and Siemer, 1968).
Low and high P supply treatments were included by applying two concentrations of P in the upper layer (0.031 and 0.310 g P L-1 nutrient solution). Thus, a P-enriched seed zone was created. The ratio between high and low concentrations of P was selected to simulate the situation in the field, with the seed zone enriched in P by a starter fertilizer and the remaining bulk soil having a lower P concentration (James and Hurst, 1995). In the bottom section, there was 0.031 g P L-1 nutrient solution.
To reduce variability between replicate seedlings, maize (‘Granat’) seeds were selected by shape and size; only seeds with a shape typical of the cultivar and with a mass within one standard deviation of the mean (225–270 mg) were used. The seeds, treated with the systemic insecticide Gaucho [1-(6-chloro-3-pyridin-3-ylmethyl)-N-nitroimidazolidin-2-ylidenamine] (Bayer AG, Zurich, Switzerland), were pregerminated on moist vermiculite in the dark at 15°C for 2 to 3 d. Seeds with a radicle 0.5 to 1 cm long were placed in a 2-cm-deep depression of 1 cm diam., which was made in the center of the top soil layer and tapered for 1 cm at the bottom of the depression where the radicle was placed. Seeds were then covered with loose substrate, and the surface of the columns was capped with the Plexiglas container described above.
Measurements
Two harvests were made: the first one at the two-leaf stage (fully expanded leaves), corresponding approximately to the transition from hetero- to autotrophic growth (Cooper and MacDonald, 1970), and the second at the three-leaf stage when the first roots reached the bottom of the lower section, i.e., the 50-cm depth. These growth stages correspond to the V2 and V3 stages of development, respectively, as defined by Ritchie et al. (1996). Within a temperature treatment, the harvest was made when 50% of the plants had reached the desired stage. The plants that grew until the three-leaf stage were irrigated with 40 mL of deionized water at the two-leaf stage.
The shoots were cut at ground level, and the fresh mass was determined. The leaf blades of the fully expanded leaves and the visible part of the leaf blade of partially expanded leaves were cut, the fresh mass determined, and the area measured with a leaf area (LA) meter (LI-COR 3100, LI-COR, Lincoln, NE).
The two fractions of shoot material, i.e., stem and leaves, were oven-dried at 65°C for 48 h, their dry masses determined and, after pooling, were ground sequentially in a sample mill (Cyclotec 1093, Tecator AB, Höganäs, Sweden) and a ball mill (Type MM2, Retsch, Arlesheim, Switzerland) to a very fine powder. After redrying, 5 mg of plant material was put into tin caps (0.04 mL, Lüdi AG, Flawil, Switzerland) and analyzed for 15N by an Integra continuous-flow mass spectrometer (Scientific Europa, Cambridge, UK) at the Stable Isotope Facility of the University of California, Davis. The shoot P concentration (Pc) was determined after dry-ashing 50 mg of plant material at 550°C for 6 h and then dissolving the ash in 1 L 20% HCl (v/v) kg-1 dry matter. Phosphorus in the solution was measured by colorimetry.
The roots of the upper and lower tube sections were washed separately under pressurized tap water, and the seeds were carefully removed. The roots were stained with fuchsin dye (Pararosaniline P-1528, Sigma Chemical Co., St. Louis, MO) for at least 12 h at 4°C, rinsed under running tap water, suspended in a thin layer of water, and evenly distributed on a glass tray, which was placed on a scanner to obtain 8-bit grayscale images (600 dpi). Because a root must be at least three pixels (dots) wide to be detected by the used image-analysis program (see below), the theoretical lower size limit of resolution was 127 µm, which is three times the pixel size of the scanner [42.33 µm at a resolution of 15.24 dots per m (600 dots per inch)].
The scanned root images were analyzed to determine the length, projected surface area, and diameter of the root objects using the computer program ROOT DETECTOR (Walter and Bürgi, 1996). The program is based on an algorithm for the segmentation and local description of elongated, symmetric line-like structures developed by Koller et al. (1995). The length and the mean diameter are computed separately for each measured root segment. Thus, the total measured root length can be sorted into user-defined diameter classes, which yields the length per diameter-class distribution of the roots. In this study, the following diameter classes were used: 0 to 200, 200 to 400, 400 to 800, 800 to 1600, and 1600 to 3200 µm. Assuming that roots have a cylindrical shape, root surface area was calculated by multiplying the measured projected area by 
. After scanning, the roots were dried at 65°C for 48 h, and their dry mass was determined.
Calculations and Statistics
Mean absolute growth rates for the dry masses of the shoot and the root and for the LA and root length were calculated by dividing the values obtained at harvest by the number of days after sowing (Hunt, 1982).
The relative contribution of N from the upper root zone to the total shoot N (%Ntop), a yield-independent parameter, was calculated as:
 | [1] |
The influx of P (or net translocation rate; Engels and Marschner, 1992) was calculated according to the following formula (Williams, 1948):
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Shoot demand per unit of root surface area was computed according to Engels and Marschner (1992) using the same formula as for P influx (Eq. [2]), whereby U was replaced by the shoot fresh mass at t = 2 and 1, respectively. Thus, shoot demand per unit of root is the rate of increase in shoot fresh mass per unit of root surface area, which gives an insight into the amount of shoot growth that has to be supplied with nutrients and water by a unit of root.
The P fertilizer utilization efficiency (PFUE) ratio was calculated according to Finck (1982) as the difference in P uptake of the shoot between the two Ptop treatments divided by the difference in the P application rate between the two P treatments.
The experimental design was a split-split plot with three replications and one plant per experimental unit. The structure of the experiment and the treatments are given in Table 1. The replicates were blocked so that there were three pairs of stacked water baths per replicate, one for each of the three temperature treatments (main-plot factor), giving nine pairs in all. Each stacked pair had 24 tubes, of which only 12 tubes were used in this experiment. The 12 tubes were necessary to test all combinations of two harvest times (subplot factor), two Ptop treatments (sub-subplot factor), and three BDtop treatments (sub-subplot factor). All results were subjected to an analysis of variance and the means separated using Fisher's protected LSD test. The level of significance for the mean separation was 
= 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Effect of Soil Bulk Density
The shoot dry mass (SDM) (Table 2) and the LA (Fig. 1)
were limited first by BDtop and second by Ptop. The effect of BDtop was highly significant at both harvests, whereas the effect of Ptop was significant at the three-leaf stage only. At the three-leaf stage, SDM (Table 2) and LA (Fig. 1) were equally high at the two lower BDtop levels (1.15 and 1.30 Mg m-3) but only with high Ptop. At low Ptop, shoot growth until the three-leaf stage tended to decrease linearly with increasing strength of the topsoil. At the highest BDtop (1.45 Mg m-3), SDM (Table 2) and LA (Fig. 1) were very small, independent of Ptop. This lower growth rate at the highest BD was associated with a markedly, but not significantly, higher Pc (Table 2), indicating that the reduced growth was probably due to more than just the limited P supply. In general, Pc was more closely related to Ptop and to the growth stage than to BDtop.
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The root/shoot ratio was affected by soil strength. At the three-leaf stage, the root area/LA ratio (Table 2), i.e., the ratio between the areas of nutrient and water absorption and C assimilation, strongly decreased with increasing resistance of the upper soil layer (Table 2). Hence, root growth was inhibited to a larger extent than shoot growth. The relative decrease in the root/shoot ratio was stronger at low than at high Ptop and more pronounced with changes in BDtop from 1.30 to 1.45 Mg m-3 than from 1.15 to 1.30 Mg m-3 (Table 2).
The proportion of total root length observed in the topsoil decreased from the two- to the three-leaf stage (Table 2). In the treatments with a BDtop of 1.45 Mg m-3, the roots did not reach the lower soil layer at the two-leaf stage, and at the three-leaf stage, root growth in the subsoil was still poor. A higher Ptop generally resulted in a greater root length, both in the topsoil and in the subsoil (Table 2). In denser topsoils (1.30 and 1.45 Mg m-3), high Ptop increased root length at the three-leaf stage to a greater extent in the subsoil compared with the topsoil; this led to a significantly lower %Ntop at 1.30 Mg m-3, i.e., a greater contribution of the subsoil to the N supply of the shoot (Table 2). In the other treatments, Ptop had no effect on %Ntop. At the two-leaf stage, >70% of N came from the topsoil, independent of BDtop, whereas at the three-leaf stage, there was a significant effect of BDtop. With a dense topsoil (1.45 Mg m-3), a larger fraction of N was taken up from the upper layer until the three-leaf stage than in case of looser topsoils (75 and 46%, respectively). The %Ntop was related to RLtop and not to the absolute root length in the topsoil (data not shown).
There was a significant interaction between BDtop and Ptop on the P influx between the two- and three-leaf stage (Fig. 2A) . At low Ptop, the influx rate was uniformly low at all BD levels, whereas at high Ptop, it increased sharply with increasing BDtop. The demand of the shoot per unit of root surface area showed the opposite tendency (Fig. 2B); it was independent of BDtop at high Ptop but not at low Ptop where it was markedly higher at 1.45 Mg m-3 compared with the lower BDtop levels.
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The Temptop did not affect the distribution of root length by diameter classes (Fig. 6) . The fraction of roots with a diameter <200 µm was approximately 10% in the topsoil at all Temptop levels (Fig. 6A) and slightly lower in the subsoil (Fig. 6B), except for the warm Temptop treatment (17.5°C). In both the upper and lower soil layers, there was a tendency towards a greater fraction of finer roots with increasing Temptop.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Topsoil bulk density was the main limiting factor for shoot and root growth. The roots were shorter and the root diameter greater with increasing BDtop, as reported by most investigators (Bennie, 1996). Total root length and total root dry mass decreased linearly with increasing BDtop, and root distribution with depth changed dramatically. The presence of a dense surface layer (1.45 Mg m-3) resulted in a concentration of roots near the soil surface; only a small fraction of the roots reached lower layers. Thus, the plants were forced to extract water and nutrients from a limited soil volume, as shown by the high %Ntop (75% at the three-leaf stage) and by a decrease in PFUE with increasing compaction of the topsoil (data not shown). However, a limited P supply was possibly not responsible for the sharp decrease in shoot growth at high BDtop (1.45 Mg m-3) and high Ptop because this growth depression was associated with a significantly higher Pc. Hence, factors other than P limited shoot growth. Several authors have mentioned an effect of soil resistance on shoot growth via root-derived hormonal signals (Masle and Passioura, 1987; Tardieu and Jensen, 1994).
Root length and root dry mass in the subsoil were affected by the strength of the topsoil as well. This might be partly due to a persistent effect of the mechanical impedance of the upper soil layer on root growth in the lower layer. When roots grow from dense soil to loose soil, the elongation rate of roots remains slower for a period of several days; possibly, cell wall properties are more important than cell turgor in regulating the elongation rate of these roots (Bengough et al., 1997). However, the main cause was probably a hindered vertical extension of the roots into the subsoil due to early maize growth in the compacted topsoil.
The diameter of the roots in the subsoil varied with the BDtop although the BD of the subsoil was the same in all treatments. This means that the mechanical impedance of the previously encountered soil layer was decisive for the root diameters in deeper soil layers. In an experiment with pea (Pisum sativum L.) in a layered soil of different penetration resistance, Bengough and Young (1993) found that the root diameter in the bottom section containing loose soil was the same in all treatments. This difference in outcome of the two experiments might be due to the different root systems of maize and pea. It was not determined in our experiment if the higher average root diameter at high BDtop was the result of a lower degree of root branching, thicker individual roots, or both. Conflicting results about the effects of mechanical impedance on overall root diameter are presented in the literature (Logsdon et al., 1987; Seiffert et al., 1995). Regardless of the reasons for thicker roots at high BDtop, plants with thicker roots are at a disadvantage as far as acquiring water and nutrients compared with plants having thinner roots because the total length of a root system with a given mass is lower with thicker than with thinner roots (Eissenstat, 1992). This is especially important in relatively dry soil and for immobile nutrients such as P.
In this experiment, Ptop was also a limiting factor for shoot growth but to a lesser degree than BDtop. Thus, only in treatments with a looser topsoil (1.15 and 1.30 Mg m-3) were plants able to take advantage of the P-enriched seed zone, as shown by the marked increase in SDM and LA at high Ptop. In general, the length, diameter, and vertical distribution of roots were influenced positively, but to a limited extent, by an increasing Ptop. Root growth was not only stimulated in the upper soil layer at high Ptop, but also in the lower soil layer, especially with dense surface layers. This can be explained by the high mobility of P within the plant (Marschner, 1995) and by the indirect effect of stimulated shoot growth and C assimilation.
The surface area of the roots per unit of LA, corresponding to the ratio between water and nutrient absorption and C assimilation area, decreased with higher BDtop, especially at low Ptop, resulting in a high shoot demand per unit of root surface area. On the other hand, the P supply from the soil at low Ptop was so limiting that an effect of BDtop on the P influx was not found, contrary to the high Ptop treatment; at high Ptop, the P influx was significantly higher in compacted soil, probably because of a better contact between roots and the soil immediately surrounding them (Veen et al., 1992) at high BDtop. Therefore, a disproportion of shoot demand per unit of root and P translocation rate from the root to the shoot (P influx) occurred at low Ptop, leading to a severe decrease in Pc (40%) from the two- to the three-leaf stage at high BDtop.
The highly significant differences in Pc between the two levels of Ptop, seen as early as the two-leaf stage, suggest that the growth substrate was the major source of P for the shoots rather than the seed. A comparison of P contents in seeds and in shoots showed that not even with a complete mobilization of seed P would the average initial P content of the seeds (486 mg P seed-1) have been sufficient to cover the P demand of the shoots. Averaged across all treatments, shoot P contents were 669 and 953 mg P plant-1 at the two- and three-leaf stages, respectively. Translocation of soil-derived P to the shoot was, therefore, already important before the two-leaf stage in this study. This is in contradiction to previous results (Barry and Miller, 1989) but can be explained by the low P concentration of the seeds in this study (on average 2 mg P g-1 seed dry mass) (O'Dell et al., 1972). Moreover, the low Pc values in plants grown at low Ptop suggest that nutrient availability limited plant growth in this case.
In agreement with published results (Walker, 1969; Barlow et al., 1976), both shoot and root growth were reduced by decreasing Temptop, despite uniform air temperatures. The tendency for a greater fraction of thinner roots as temperature increased also agrees with previous studies (Stamp, 1983; Cutforth et al., 1986). However, contrary to the literature (Engels and Marschner, 1990), no change in the shoot/root surface ratio was observed, probably as a result of the narrow range of tested soil temperatures (Walker, 1969).
In general, shoot growth at suboptimal root temperature can be limited both by a direct temperature effect on the shoot meristem and by a reduced nutrient supply through the roots (Engels and Marschner, 1990). According to Walker (1969), who reported statistically different dry masses of roots and shoots of maize seedlings when soil temperatures differed by only 1 or 2°C, a direct effect of temperature most certainly occurred here.
A temperature-induced reduction in the nutrient supply through the roots can be due to effects on (i) the uptake efficiency per unit of root length (Bravo and Uribe, 1981; Mackay and Barber, 1984); (ii) the growth, morphology, or distribution of the roots (Engels and Marschner, 1992); and (iii) the supply of nutrients by the soil (Marschner, 1995). The latter was probably not the case at the temperatures tested here, and thus will not be discussed. As far as (i) is concerned, temperature did not seem to affect the P influx in this study. Moreover, temperature did not appear to affect the demand of the shoot per unit of root, indicating that the shoot and the roots were similarly influenced by the Temptop. This was also shown by the fact that the shoot/root ratio did not change with soil temperature. Engels and Marschner (1992) reported a disproportion of shoot demand per unit of root and P influx in treatments where a low root-zone temperature was combined with a high shoot base temperature but not in the treatments in which the temperature of the root zone and shoot base was uniform as in our study. The positive effect of a higher Temptop on root growth [see (ii) above] resulted in a higher PFUE (data not shown) and higher Pc values at the two-leaf stage. At the three-leaf stage, however, there was a tendency towards lower Pc values in the warmer treatments. This is an additional confirmation that low soil temperature in a range simulating spring conditions does not necessarily limit growth by reducing P uptake, as concluded by Walker (1969). Engels (1993) also found a slight decrease in Pc with increasing root temperature in 3-wk-old maize, but others found the reverse (Grobbelaar, 1963) or no effect (Patterson et al., 1972). The reasons for this inconsistency are not yet clear but may be related to the different varieties of maize, rooting media, climatic conditions, and the soil temperature treatments in these studies. Furthermore, higher soil temperatures may compensate for a lower level of soil P, and vice versa, as shown by the interaction between Temptop and Ptop on root growth (Table 3) and as suggested by Mackay and Barber (1984).
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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To summarize, our study clearly demonstrates the importance of P supply through the roots for the growth of maize seedlings, already before the two-leaf stage. Phosphorus concentration in the shoot tissue was mainly determined by P availability in the growth substrate and P dilution by growth.
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