JXB Advance Access originally published online on July 28, 2003
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Journal of Experimental Botany, Vol. 54, No. 390, pp. 2105-2109,
September 1, 2003
© 2003 Oxford University Press
Root cap removal increases root penetration resistance in maize (Zea mays L.)
Received 28 February 2003; Accepted 29 May 2003
1 Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan
2 School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
3 Scottish Crop Research Institute, Dundee DD2 5DA, UK
* To whom correspondence should be addressed. Fax: +81 52 789 4012. E-mail: miijima{at}agr.nagoya-u.ac.jp
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Abstract |
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The root cap assists the passage of the root through soil by means of its slimy mucilage secretion and by the sloughing of its outer cells. The root penetration resistance of decapped primary roots of maize (Zea mays L. cv. Mephisto) was compared with that of intact roots in loose (dry bulk density 1.0 g cm–3; penetration resistance 0.06 MPa) and compact soil (1.4 g cm–3; penetration resistance 1.0 MPa), to evaluate the contribution of the cap to decreasing the impedance to root growth. Root elongation rate and diameter were the same for decapped and intact roots when the plants were grown in loose soil. In compacted soil, however, the elongation rate of decapped roots was only about half that of intact roots, whilst the diameter was 30% larger. Root penetration resistances of intact and decapped seminal axis were 0.31 and 0.52 MPa, respectively, when the roots were grown in compacted soil. These results indicated that the presence of a root cap alleviates much of the mechanical impedance to root penetration, and enables roots to grow faster in compacted soils.
Key words: Border cell, decapping, mucilage, root cap, root growth pressure, soil compaction.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The root cap protects the root meristem from abrasion by soil particles. It has also been suggested that it reduces soil mechanical impedance by means of its secretion of slimy mucilage and by the sloughing of border cells (Iijima and Kono, 1992; Bengough and McKenzie, 1997; Iijima et al., 2000). However, the degree to which the mechanical impedance to root growth is reduced by the presence of the root cap is not known.
Those plant species with a closed-type meristem, such as maize (see Fig. 3A in Bengough et al., 2001), have a clearly demarcated boundary between the root cap and the root proper. One consequence of this is that the cap can be easily removed from the root tip. To date, removal of the root cap (decapping) has been used to investigate the regeneration process of the root cap (Barlow, 1974; Barlow and Sargent, 1978; Barlow and Hines, 1982), the reactivation of cells in the quiescent centre (Grundwag and Barlow, 1973; Müller et al., 1994), aluminium toxicity (Schofield et al., 1998), and the role of the root cap as a sensory organ for perceiving mechanical (Goss and Russell, 1980) or gravitational stimuli (Pilet, 1971; Barlow, 1974; Stinemetz, 1995). This decapping technique could potentially be used for testing various other roles of the root cap: for example, whether or not the root cap reduces root penetration resistance. Root penetration resistance is the reaction force exerted by the soil on the penetrating root per unit root cross-sectional area (Bengough and Mullins, 1990). Root penetration resistance has been directly measured in a number of studies (Stolzy and Barley, 1968; Whiteley et al., 1981; Bengough and Mullins, 1991). In this paper, a comparison of the root penetration resistance of decapped and intact roots was used to evaluate the role of the root cap in alleviating soil mechanical impedance.
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Materials and methods |
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Seed germination and soil preparation
Maize (Zea mays L. cv. Mephisto) seedlings were used for the experiments. This variety of maize has a cap which is easily removed, and has been used previously in root penetration resistance experiments (Iijima et al., 2000). Maize caryopses were surface-sterilized by immersion in a saturated solution of calcium hypochlorite for 5 min. They were then washed several times with distilled water and allowed to germinate on blotting paper moistened with distilled water in a Petri dish, in darkness, at 23 °C for 72 h. Seedlings with a straight seminal root, 20–35 mm long, were used in all experiments.
Sandy loam soil (sand 56%, silt 36%, clay 8%) was sieved through a 2 mm mesh, and then wetted to a water content of 23.6 g water per 100 g soil (matric potential approximately –5.4 kPa). The soil was kept in a plastic bag prior to packing.
Experiment 1: effects of decapping and soil compaction on root elongation and diameter
First, the effect of decapping upon root growth in length and diameter was tested. The wetted soil was packed in layers, using a metal plunger and compressor, into plastic tubes (100 mm height, 60 mm diameter) at soil bulk densities of 0.8 Mg m–3 or 1.4 Mg m–3 (air-filled porosity 0.14 cm3 cm–3), and here termed ‘loose’ and ‘compact’, respectively. A sharp scalpel blade was used to decap the roots, following the method used by Barlow and Hines (1982), and those seedlings from which the root cap came off cleanly were selected (Fig. 1). Four seedlings, with known root length, were transplanted into each plastic cylinder. After 24 h growth in darkness at 23 °C, the roots were excavated gently and their lengths measured. Diameters at 1–4 mm behind the root apex were measured using a stereo microscope with an eyepiece graticule. In total, 9–12 replicate plants were grown in the two bulk densities and decapping or intact root treatments.
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Experiment 2: root penetration resistances
Initial root diameters were measured 2, 3, 4, and 5 mm behind the apex of both decapped and intact seminal roots under the stereomicroscope. After this the plants were transferred to the seedling holder (50 mm height, 30 mm diameter) illustrated in Fig. 2. The seminal root axis was held vertically and anchored rigidly behind the zone of elongation. The air gap between the root holder and the soil core surface was made as small as possible to minimize the chance of the root buckling and any drying of the root surface. The distal 1 mm of root tip was inserted into a narrowly tapered hole (2 mm deep) in the surface of the soil core. Compact cores (50 mm height, 50 mm diameter) were used with the same bulk densities as in experiment 1. The resistance experienced by the root tip in the loose soil type was considered to be too small to evaluate the difference between decapped and intact roots accurately. Hence, only the root penetration resistances obtained by penetration into the compact soil are reported here. The root was fixed in position with a small quantity of plaster of Paris, and the whole seedling was covered loosely with the wetted soil. One seedling was transplanted into each root holder and allowed to grow for a further 20–22 h at 23 °C in darkness. In total, 10 replicate plants were grown in the decapping and intact root treatments. The soil core was set on an electric balance so that the pushing force of the root into the soil core was recorded as the ‘root force’. Balance readings (accurate to within 0.01 g) were taken automatically every 10 or 30 min during the 20–22 h growth period by means of a personal computer interfaced to the balance output. After this, the root was excavated from the soil core, and the final root diameters were measured at the locations mentioned, and compared with the initial diameters. The root penetration resistance (Q) was calculated as
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where F is the root force and A is the average cross-sectional area of the root at 2, 3, 4, and 5 mm behind the apex.
Penetrometer resistance
Penetrometer resistance of the soil core was measured using a 0.98 mm diameter probe with a 30° cone angle. The probe was pushed into the soil core at a rate of 1 mm min–1 from the soil surface to depths of 10 mm or 20 mm in the cases of compact or loose soils, respectively. The penetrometer resistance was calculated according to equation 1, substituting penetrometer force for root force, and the maximum cone cross-sectional area for root cross-sectional area. Three such penetrometer tests were made in the loose and compact treatments of experiment 1, and for the compact treatment in experiment 2.
Statistical analysis
In experiment 1, differences among the treatments were subjected to a two-way analysis of variance (2-way ANOVA), then Duncan’s multiple range test was applied to compare means among the four treatments. In experiment 2, differences between the two treatments were subjected to a one-way analysis of variance (1-way ANOVA).
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Experiment 1: effects of decapping and soil compaction on root elongation and diameter
Penetrometer resistance of the soil used in experiment 1 was 0.06 MPa for loose, and 1.06 MPa for compact treatments, respectively. Decapping did not alter the elongation rate nor the root diameter in the loose treatment (Table 1). In this experiment, using intact roots, the compact soil treatment reduced root elongation by 44% and increased root diameter by 17% (Table 1). By contrast, elongation rates of decapped roots in compact soil showed 71% lower elongation rates and 52% thicker diameters than those of the loose treatment. In both root elongation rates and diameter, interactions between the decapping and compaction treatments were significant at P <0.01, therefore, treatment means were subjected to the Duncan’s multiple range tests. The decapped roots were significantly more sensitive than intact roots to the effect of mechanical impedance.
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Experiment 2: root penetration resistances
Penetrometer resistance increased initially during the first 3 mm of penetration, and then plateaued (Fig. 3). Root elongation rate was assumed constant in the calculation (as in Bengough and Mullins, 1991), and root diameter was assumed to increase linearly with time. Root penetration resistance increased to a depth of 6 mm and then plateaued for the decapped roots, with a continued gradual increase for the intact roots. The root penetration resistance was evaluated when the root tip was estimated to be between 3 mm and 6 mm below the soil surface. This was sufficient to eliminate soil surface deformation effects, but before the root became anchored by root hairs. Root force doubled, and root penetration resistance was increased by 68% in roots that had their caps removed (Table 1). Thus, decapped roots experienced greater mechanical impedance than intact roots.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Removal of the root cap increased the root force and root penetration resistance substantially (Table 1). This increased mechanical impedance to root growth resulted in slower root elongation (12 mm d–1 in decapped roots, 22 mm d–1 in intact roots), and increased thickening in the decapped roots (1.61 mm diameter compared with 1.06 mm). The lack of any effect of decapping on elongation rate and diameter in the loose soil suggests that decapping per se did not cause these changes. In other words, the mechanical impedance of loose soil, 0.06 MPa, used in this experiment was too small to slow root elongation growth. Generally speaking, field soils exhibit larger mechanical impedance than this, unless roots are growing in continuous pores or a newly-tilled seed bed at near field capacity. The root cap is thus generally important to reduce soil mechanical impedance except in the case of such loose soil conditions.
Root penetration resistance is the sum of the frictional resistance to root penetration, plus the pressure required to form a cavity in the soil (Greacen et al., 1968; Bengough and Mullins, 1990, 1991). The cause of the increase in root penetration resistance may, therefore, be due to changes in the frictional resistance to root penetration or changes in the pressure required to expand a cavity in the soil resulting from a change in the shape of the root tip. The decapping experiments performed cannot differentiate between these two components of penetration resistance, although it is possible to consider their relative importance.
A possible reason for the increase in root penetration resistance on decapping is the decrease in root cap border cell production and the exudation of mucilage. In compacted sand, Iijima et al. (2000) estimated that the whole surface of the root cap might be covered in detached border cells. Exudation of mucilage may also be increased by soil compaction (Barber and Gunn, 1974; Boeuf-Tremblay et al., 1995; Iijima and Kono, 1992; Iijima et al., 2000). By removing the bulk of the root cap, including the cap meristem, border cell and mucilage production is effectively restricted to the small portion of the remaining lateral cap (see Fig. 3A of Bengough et al., 2001). This means that friction will occur directly between soil particles and cells of the root proper, with a much diminished lubricating layer of mucilage or border cell-mucilage sandwich. By 24 h after decapping, mucilage production would begin again in the outer cells of the decapped apex (Barlow, 1974; Barlow and Sargen, 1978), but this is beyond the timescale of these experiments.
It is also possible that the blunter shape of the decapped root will increase root penetration resistance. In the case of metal probes with cone-angles of 30°–60°, however, the penetration resistance was relatively unaffected by cone-angle (Gill, 1968). Probes with narrow cone-angles tend to deform the soil cylindrically, whilst blunter probes cause more spherical soil deformation (Greacen et al., 1968; Bengough et al., 1997). The reality for roots probably lies somewhere between the cylindrical and spherical extremes, and it is likely that the decapped blunter roots will tend further towards the less efficient spherical mode of deformation.
Root penetration resistance was smaller than penetrometer resistance, even in the case of the decapped roots. This may be due to a combination of the root–soil friction being smaller than the soil–metal friction, but also to the faster rate of penetration of the penetrometer probe (some 65–120 times faster). Although penetration resistance is not strongly dependent on rate, this may well account for some of the difference between root and penetrometer resistance.
In conclusion, this study has provided new direct evidence that root caps facilitate root penetration, enabling faster root elongation in compact soils. The mechanism for this probably involves border cell and mucilage lubrication of the root–soil interface, coupled with the tapering shape of the root cap.
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Acknowledgements |
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We thank the Japanese Society of Promotion of Science (B2-12460010) and the Royal Society for funding the visit to SCRI and IACR Long Ashton by Dr Iijima and Mr Higuchi. The Scottish Office Agriculture, Environment and Fisheries Department provide grant-in-aid to SCRI. Thanks to Blair McKenzie for helpful discussions.
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References |
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