AOBPreview originally published online on December 22, 2005
Annals of Botany 2006 97(5):867-873; doi:10.1093/aob/mcj605
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Influence of Inorganic Nitrogen and pH on the Elongation of Maize Seminal Roots
1 Department of Plant Sciences, University of California, Davis, CA 95616, USA, 2 Cyberonics Europe S.A./N.V., Belgicastraat 9, 1930 Zaventem, Belgium and 3 Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
* For correspondence. E-mail ajbloom{at}ucdavis.edu
Received: 8 August 2005 Returned for revision: 28 September 2005 Accepted: 15 November 2005 Published electronically: 22 December 2005
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims Root absorption and assimilation of inorganic nitrogen usually alters rhizosphere pH, but the immediate influence of such pH changes on root elongation as well as that of exogenous inorganic nitrogen itself has been uncertain.
• Methods A differential extensiometer that monitored on a real-time, continuous basis root elongation in an intact 3-d-old maize plant was developed. Treatments included root media at pH 6·5 or 5·6 that lacked nitrogen and ones at pH 6·5 that contained 100 mmol m–3 
or 
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• Key Results Acidifying the root medium from pH 6·5 to 5·6 nearly doubled the elasticity of the seminal root, but slightly decreased its elongation. Plasticity of the root apex was not detectable in all treatments. The presence of ammonium or nitrate in the medium stimulated elongation by 29 % or 14 %, respectively. Addition of an osmoticum to the medium had no effect on root elongation in the absence of inorganic nitrogen, but diminished the stimulation of elongation in the presence of ammonium and nitrate. This indicates that these ions or their by-products serve partially as osmolytes.
• Conclusions In nutrient solution, root elongation of a maize seedling—even one with ample nitrogen reserves—depended most strongly on exogenous inorganic nitrogen, and less so, if at all, on either the pH of the bulk nutrient solution or the mechanical properties of cell walls.
Key words: Nitrate, ammonium, rhizosphere pH, Zea mays, acid growth, cell wall elasticity, root growth, nutrient solution, turgor pressure, osmotic potential
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INTRODUCTION |
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The below-ground environment from which plants extract nutrients and water is highly heterogeneous, both spatially and temporally. For example, inorganic nitrogen concentrations in a soil may range a 1000-fold over a distance of centimetres or over the course of hours (Bloom, 1997b
). Given such heterogeneity, plants depend on various tropisms (e.g. gravitropism, thigmotropism, hydrotropism and, perhaps even, chemotropism) to guide root growth toward soil resources (Epstein and Bloom, 2005). The physiological mechanisms through which these tropisms alter growth remain uncertain, although the ‘acid growth hypothesis’ is often raised as a possibility (e.g. Chen et al., 2002; Peters, 2004).
According to the ‘acid growth hypothesis’, plants regulate cell expansion through modifying the pH around the cell wall and thereby its extensibility, which increases at low pH (Cosgrove, 1999). A large body of evidence supports this hypothesis in shoot coleoptiles or expanding leaves (Rayle and Cleland, 1992; Peters et al., 1998; Van Volkenburgh, 1999; Kotake et al., 2000; Schopfer, 2001; Friml, 2003), but results on roots have been less conclusive. Lowering the pH of the medium may either promote root elongation (Edwards and Scott, 1974; Evans, 1976; Winch and Pritchard, 1999) or have little effect (Büntemeyer et al., 1998; Peters and Felle, 1999; Walter et al., 2000). The standard approach for examining the influence of pH on cell extension has been to examine tissue segments subjected to severe treatments: for example, in Wu et al. (1996), frozen root segments were abraded with carborundum, thawed and squeezed between two glass slides to remove cell sap; in Tanimoto et al. (2000), lateral roots were killed in boiling methanol; and in Schopfer (2001), the segments were frozen, thawed, and abraded. Such treatments have been deemed necessary because the mechanical properties of cell walls in fresh, turgid tissue could be complex (D. J. Cosgrove, pers. comm.).
Rhizosphere pH changes as roots absorb and assimilate inorganic nitrogen; the assimilation of strongly acidifies, whereas absorption of slightly alkalizes the media near the root apex (Smart and Bloom, 1998; Taylor and Bloom, 1998). These rhizosphere pH changes may be responsible for the differential patterns of root growth observed under vs. nutrition (Bloom, 1997a; Bloom et al., 2002). Alternatively, and themselves may be responsible for the root developmental responses (Forde, 2002).
To test the acid growth hypothesis in roots and the short-term influence of exogenous inorganic nitrogen on root elongation, a new approach was developed that provides measurements of the mechanical properties and elongation of the root apex on a real-time, continuous and non-destructive basis. Here it is reported that, in this device, exposure of a maize seminal root to a more acid medium dramatically enhanced its elasticity, but factors such as the availability of inorganic nitrogen in the medium had a greater influence on root elongation than cell wall mechanical properties.
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MATERIALS AND METHODS |
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Maize (Zea mays L. cv. WF9 x Mo17) seeds were placed on germination paper (thick, fine weave, paper towelling) soaked in 1·0 mol m–3 CaSO4 for 2 d and transferred to a 0·004 m–3 light-impervious polyethylene container filled with an aerated nutrient solution containing 0·15 mol m–3 NH4NO3, 1 mol m–3 CaSO4, 0·5 mol m–3 K2HPO4, 0·5 mol m–3 KH2PO4, 2 mol m–3 MgSO4, 0·2 kg m–3 Fe-NaEDTA, and micronutrients according to Epstein and Bloom (Epstein and Bloom, 2005
). The containers were placed in a controlled environment chamber that provided a photosynthetic photon flux density of 400 µmol m–2 s–1 at plant height for a 14 h light period at 25 °C and a 10 h dark period at 15 °C.
The next day, a plant whose seminal root was 120–180 mm in length was placed into an extensiometer [for a black and white illustration of this, see fig. 3 in Bloom et al. (2002) or, for one in colour, fig. 9.5 in Epstein and Bloom (2005)]. The seedling was supported in the extensiometer by its caryopsis. The seminal root lay against a surface of the extensiometer that was tilted 4 ° from vertical. The side walls of the extensiometer extended outward from the surface to form a trough. A nutrient solution flowed down this trough, bathing the root. The solution contained 1 mol m–3 CaSO4, 200 mmol m–3 KH2PO4 and either 100 mmol m–3 NH4H2PO4, 100 mmol m–3 KNO3, or no nitrogen, and was adjusted to pH 6·5 or 5·6 with KOH. The osmotic potential of these solutions was –0·082 MPa. Their pH was continuously monitored throughout an experiment and did not vary >0·2 pH units. At the midpoint of an experiment, 68 mOsm KCl (
s = –0·14 MPa) was added to assess the response of the root elongation to a shift in osmotic potential. The end of a small plastic pipette tip was cut off, a large knot tied in one end of a nylon thread, the free end of the thread passed through the narrow opening of the pipette tip, the tip attached to the root cap with surgical-grade cyanoacrylic glue, and the other end of the thread tied to an arm connected to the shaft of a rotary variable inductance transducer (RVIT; Schaevitz 15–60, Pennsauken, NJ, USA). Weights of 1·2, 2·4, 3·6 and 5·2 g were placed on this arm to stretch the root and assess its elasticity plus plasticity and then were removed to assess elasticity alone. Applying a weight of 5·2 g was approximately equivalent to subjecting the root to an osmotic potential of –0·14 MPa [based on F = P x A, where F = force, P = pressure and A = surface area, and given that the roots had a radius of about 0·5 mm and an effective cross-section of 5 % as estimated from measurements of root hydraulic conductance (Frensch and Steudle, 1989); and from micrographs of the apex (Bloom et al., 2002)]. Five minutes or longer were allotted after addition or removal of weights to permit the elongation of root apex to resume a steady rate (Fig. 1). A small piece of a wooden toothpick was glued to the root initially about 14 mm from the apex, a part of the root that is no longer elongating (Taylor and Bloom, 1998). A nylon thread connected this toothpick to a linear variable differential transducer (LVDT, Schaevitz 050 DC-D). A two-channel chart recorder logged the output from the RVIT and LVDT.
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A flat-bed scanner and an image analysis program (Digitize-Pro, Dr Yaron Danon) digitized the chart recorder tracings. Apical root length was taken as the difference in the positions of RVIT and LVDT. After smoothing the data using a Gaussian kernel to compute local weighted averages, the elongation rate was calculated from the changes in length over time through numerical differentiation (Mathcad 12, Mathsoft). An FIR (finite impulse response) high-pass filter (Mathcad 12, Mathsoft) was also used to assess the sudden shifts in length when weights were added or removed. An ANOVA (General Linear Model; CoStat, CoHort Software) was used to test for significant differences among means (P < 0·05).
Neumann used a similar approach to examine the influence of NaCl (Neumann, 1993), polyethylene glycol (Chazen and Neumann, 1994) and nutrient supply (Snir and Neumann, 1997) on leaf extension, but employed a single transducer. Consequently, his extensiometer monitored the leaf as a whole and did not isolate the changes in a specific region. In the present study, to monitor the elongation of just the root apex and to eliminate any signal generated from movement of the whole plant when weights were added, the difference between two transducers was monitored.
To determine segment mass, and concentrations and osmotic potential along the maize root, individual seedling roots were exposed to the various nitrogen treatments for 18–24 h, and gently blotted dry before they were rapidly (<2 s) frozen on a thermoelectric cold-plate mounted under a dissecting microscope. Axial sections of 1 mm length were made with a fine razor blade at 1-mm increments from 1 to 10 mm from the apex along each of ten roots. Root sections from each location were oven-dried and weighed to determine dry mass per unit length. Other root sections from each location were pooled and collected in Eppendorf tubes containing 1·5 ml of 1 mol m–3 CaSO4, which was adjusted to pH 3 with H2SO4. These sections were sonicated for 30 min and then centrifuged. The supernatant was withdrawn and analysed for and as described below. There were at least three replicates for each N-treatment. Root and contents were expressed per segment water volume based on root radius measurements at each location. Two other frozen root sections from each location were immediately placed after excision into the sample chamber of a Wescor 5100 thermocouple psychrometer (Logan, UT, USA) to assess osmotic potential.
To analyse concentrations in the samples, a fluorimetric method based on the reaction of with o-phthalaldehyde (OPA) was modified (Goyal et al., 1988). An autosampler (Shimadzu Sil 9-A, Japan) injected a 50 mm3 sample into the flow of a buffer solution consisting of 126 mol m–3 K2HPO4, 74 mol m–3 KH2PO4, 5 mol m–3 OPA and 0·39 dm3 m–3 ß-mercaptoethanol. The stream circulated for several minutes through a cabinet controlled at 64 °C to optimize the -OPA reaction. The -OPA in each sample was quantified using a fluorescence detector (Shimadzu RF-551, Japan) set at 410 nm excitation and 470 nm emission. The time from sample injection to peak detection was 3·4 min with a pump flow rate of 2 cm3 min–1.
Analysis of was conducted via HPLC (Thayer and Huffaker, 1980). Samples of 50 mm3 were injected into a stream of 35 mol m–3 KH2PO4 (adjusted to pH 3·0 with H3PO4) before passing into a 100 mm x 4·6 mm column packed with anion exchange resin (Partisil Sax 10 mol m–3; Whatman Laboratory, USA). The absorbance of column eluent was monitored at 210 nm. The time from sample injection to peak detection was 1·8 min.
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RESULTS |
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Elongation rates of the seminal root after placing a 3-d-old maize seedling into an extensiometer equipped with two high-resolution position transducers became uniform in about 1 h (data not shown) and remained so for several hours (Fig. 1). These rates ranged from 1·5 to 2·2 mm h–1 (Figs 1 and 2), values similar to those reported for seminal roots of well-watered maize growing in vermiculite (Sharp et al., 1990
), in solution culture (Frensch and Hsiao, 1994; Taylor and Bloom, 1998; Winch and Pritchard, 1999) or along germination paper (Bloom et al., 2002). Recovery to steady rates required <5 min after addition or removal of weights and <15 min after the addition of 68 mOsm KCl (Fig. 1). These findings indicate that the procedures used were benign and did not significantly damage the root.
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Elongation of the seminal root in the nitrogen-free nutrient solution was slightly faster at pH 6·5 than at pH 5·6 (Fig. 2). Providing 100 mmol m–3
or 100 mmol m–3 in the nutrient solution at pH 6·5 stimulated elongation by 29 % or 14 %, respectively, in comparison with the nitrogen-free solution at the same pH (Fig. 2). The addition of 68 mOsm KCl had little effect on elongation in the nitrogen-free solutions, but decreased the rates under or by 7 % and 18 %, respectively (Fig. 2).
The stretching of the seminal root was proportional to the weight applied (Fig. 1) and the root fully recovered when the weights were removed (Fig. 3). This shows that the stretching response of the root apex was predominantly elastic, not plastic. Root elasticity in the more acidic solution (pH 5·6) was double that in the more neutral solution (pH 6·5). In the neutral solution, root elasticity was insensitive to nitrogen treatment (, or nitrogen-free) and the presence or absence of 68 mOsm KCl (Fig. 3).
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The mass of root segments were slightly higher in the more mature root zones of plants receiving 100 mmol m–3
than in those receiving 100 mmol m–3 (Fig. 4). Concentrations of near the root apex were slightly higher in the plants receiving 100 mmol m–3 than in those receiving a nitrogen-free medium (Fig. 4A). By contrast, concentrations were negligible in the plants receiving nitrogen-free medium, but increased to over 14 mol m–3 in the more basal parts of the root in the plants receiving 100 mmol m–3 (Fig. 4B). The overall osmotic potential of the apex (mean ± s.e.) did not vary significantly among the nitrogen treatments (–1·13 ± 0·06 MPa for the , –1·05 ± 0·05 MPa for the , and –1·17 ± 0·07 MPa for the nitrogen-free), and the values observed were similar to those previously reported for maize root apices (Sharp et al., 1990).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The acid growth hypothesis of roots, although well-known, has been subject to only limited experimental testing with only seven studies that have focused on this topic (Edwards and Scott, 1974
; Evans, 1976; Büntemeyer et al., 1998; Peters and Felle, 1999; Winch and Pritchard, 1999; Tanimoto et al., 2000; Walter et al., 2000). Of these studies, several only examined elongation of root segments (Edwards and Scott, 1974; Büntemeyer et al., 1998; Tanimoto et al., 2000) or subjected the roots to relatively large pH changes [pH 6·5–4·0 (Evans, 1976); pH 7·0–3·4 (Winch and Pritchard, 1999)]. The present results for root apices of intact plants demonstrate that even moderate changes in rhizosphere pH (between pH 6·5 and 5·6) can dramatically influence the elasticity of the apex (Fig. 3), but that this may not influence the elongation of this region (Fig. 2). By contrast, the presence of exogenous inorganic nitrogen significantly enhanced elongation (Fig. 2), even though the seedlings had ample nitrogen reserves in the caryopsis to support growth for several more days (Bloom et al., 2002).
The meristem and transition zones (Baluska et al., 1996) near the root apex differ from more mature root zones in that they lack fully differentiated phloem tissue. Import of carbohydrates or some nutrients (e.g. K+) from more mature tissues into the root apex may depend on diffusion through the symplast (Bret-Harte and Silk, 1994b) or may be enhanced by pressure driven flow from sieve tube elements (Boyer and Silk, 2004; Gould et al., 2004). Nevertheless, little of the nitrogen absorbed in the maturation zone moves toward the apex (Siebrecht et al., 1995; Walter et al., 2003); therefore, the nitrogen required for cell division and isotropic cell expansion may derive primarily from nitrogen that the apical zones themselves absorb and assimilate.
The stimulation of root elongation in the presence of exogenous or is an appropriate response with ecological implications (Bloom, 1997a). Plants predominantly obtain nitrogen through root absorption of and from the soil solution (Bloom, 1997b). Spatial and temporal availability of soil inorganic nitrogen is highly heterogeneous, as mentioned above. To survive under such heterogeneity and under competition from soil microorganisms, plant roots must be in the right place at the right time. Appropriately, roots proliferate in soil regions that are nitrogen-rich (Hackett, 1972; Drew, 1975; Grime et al., 1986; Sattelmacher and Thoms, 1989; Bingham et al., 1997; Robinson et al., 1999; Zhang et al., 1999). Specifically, proliferation of lateral roots seems critical for exploiting nitrogen-rich regions (Bloom et al., 2002; Forde, 2002). The phenomenon observed here—acceleration of seminal root elongation by exogenous inorganic nitrogen—would rapidly position the mature zones of seminal roots, from where lateral roots emerge, adjacent to nitrogen-rich soil regions.
The presence of stimulated root elongation (Figs 2 and 3) and accumulation of root biomass (Fig. 4) to a greater extent than that of . This is consistent with other studies (Bloom et al., 1993) and may reflect that assimilation of to glutamine consumes the equivalent of about 2 ATPs per , whereas assimilation of to glutamine consumes the equivalent of about 12 ATPs per (Bloom et al., 1992). In the carbohydrate-limited apical meristem (Bret-Harte and Silk, 1994a), the lower energy requirement for assimilation may permit cells to maintain higher elongation rates and to accumulate more biomass.
Diminishing the osmotic potential of the nutrient solution from –0·08 to –0·22 MPa by the addition of 68 mOsm KCl had no effect in the nitrogen-free treatments, but depressed root elongation under and nutrition (Fig. 2). In maize, apical zones of the root rapidly absorbed and (Taylor and Bloom, 1998). Most of the absorbed promptly disappeared from the tissues (Fig. 4A), presumably, as it was assimilated into amino acids (Bloom et al., 2002). Some of these amino acids may serve as metabolically benign osmolytes to support cell expansion in the elongation zone (Rhodes et al., 2002). By contrast, a portion of the absorbed remained as free within the apical zones (Fig. 4B), providing another metabolically benign osmolyte (up to 29 mOsm or –0·063 MPa) to support expansion (Bloom, 1996; Bloom, 1997a; McIntyre, 2001). The addition of 68 mOsm KCl to the nutrient solution depressed root elongation possibly because it counteracted the osmotic effects of the stored amino acids and . Although the osmotic potential resulting from the amino acids, or KCl was small in comparison to the total osmotic potential of the apex (1·1 MPa), these metabolically benign osmolytes were probably not distributed evenly throughout the root, but concentrated in the more metabolically active compartments (Aspinall and Paleg, 1981).
It is unlikely that the effects of 68 mOsm KCl on the plants receiving or were specific to the ions K+ and Cl–. The high-affinity transport systems for and , which predominate at 100 mmol m–3, are insensitive to the presence of K+ (Scherer et al., 1984; Bloom and Finazzo, 1986; Smart and Bloom, 1988; Bloom and Sukrapanna, 1990) or Cl– (Glass et al., 1985; Bloom and Finazzo, 1986; Deane-Drummond, 1986). In previous experiments on maize roots, mannitol and KCl were indistinguishable in their effects on cell turgor and root elongation (Frensch and Hsiao, 1995). Neither elasticity nor plasticity of the root apex changed with the addition of 68 mOsm KCl (Fig. 3), and thus cell wall properties seemed unresponsive to additions of these ions.
In Lockhart's model (Lockhart, 1965), the rate of cell expansion depends upon its extensibility times its turgor pressure in excess of a certain threshold [RGR = m x (Pc – Y), where RGR is cell relative growth rate, m is volumetric extensibility, Pc is cell turgor pressure and Y is yield threshold turgor pressure]. Cell wall elasticity and plasticity were assessed by rapid shifts in root length produced by the addition or removal of weights. Cell wall elasticity at pH 5·6 was nearly doubled from the value at pH 6·5; plasticity was negligible under all treatments (Fig. 3). Such shifts might derive from either stretching cell walls or altering cell turgor. For example, if cells growing at pH 5·6 had less turgor than those at pH 6·5, then stretching could occur more easily, independent of cell wall extensibility.
Winch and Pritchard (1999) examined maize at the same age as the plants in the present study and grown under similar conditions. They found that cell turgor pressures were similar in roots exposed to pH 7·0 and 3·4. Presumably, cell turgor pressures remained unchanged over the narrower pH range of 6·5–5·6 used in the present experiments. Therefore, the responses to mechanical perturbation that were observed were derived primarily from changes in cell wall elasticity of the root apex. That the root apex responds in primarily an elastic fashion seems reasonable. Cell walls are reinforced in the maturation zone, a region basal to the one examined in the present study; thus, the maturation zone presumably would demonstrate more of a plastic response with irreversible increases in length.
Elongation of the root apex was compared at pH 6·5 and 5·6, a pH range found in the soils around Davis, California (DeClerck and Singer, 2003). Maize yields are relatively insensitive to soil pH in this range (McLean and Brown, 1984). A change from pH 6·5 to 5·6 doubled the elasticity of maize roots (Fig. 3), but slightly slowed root growth (Fig. 2). These results indicate that cell wall properties alone do not regulate root elongation.
Some researchers have questioned whether cell wall mechanical properties can be measured on live, turgid tissue because walls suffering both strain in all directions due to turgor and strain in a unidirectional vector due to the addition of weights might behave in a complex manner. Nonetheless, it was found that roots of intact plants exhibited simple mechanical properties; elongation was linear with the strain applied (Fig. 1) and recovery from the strain was complete (Fig. 3). These results permit a simple interpretation.
Proton pumps in the apical zones of roots generate what are known as ‘growth currents’ that have an important role in the determination and regulation of root polarity (Weisenseel et al., 1979; Miller and Gow, 1989). A previous study (Taylor and Bloom, 1998) found that maize roots exposed to either 100 mmol m–3 , 100 mmol m–3 , or nitrogen-free media pumped sufficient protons to maintain the root surface in the elongation zone at least 0·4 pH units more acidic than the bulk solution; the greatest pH differentials, however, were in the nitrogen-free treatment. These results indicate that the differences in root elongation observed in the current study were not simply that the various nitrogen treatments produced different pHs in the elongation zone.
Walter et al. (2003) reported that elongation of maize roots was faster in pure water than in a nutrient solution containing both and , a finding contradictory to those presented here. This solution, however, provided at 3·85 mol m–3, a concentration several times higher than the highest levels measured in agricultural fields in Davis, California (Jackson and Bloom, 1990), and the maize roots grown in this solution accumulated high levels of free (40 µmol g–1) in the meristems. For comparison, in the present study, the nutrient solution used contained 0·1 mol m–3 , and free concentrations in the root meristems were <6·7 µmol g–1 (Fig. 4A, calculated on the basis that root segments were 87 % water). High accumulations of free in tissues are toxic because they dissipate pH gradients in mitochondria and plastids (Epstein and Bloom, 2005). Thus, toxicity might explain the differences between the results of the two studies.
In summary, the results of the present study indicate that in well-watered maize plants, exogenous inorganic nitrogen more than pH or cell wall elasticity or plasticity influences the elongation of the root apex.
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ACKNOWLEDGEMENTS |
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We thank T. C. Hsiao for the use of equipment, and T. C. Hsiao and Nigel Crawford for their comments on the manuscript. This work was supported in part by the USDA NRICPG Grant 2000-00647 and National Science Foundation Grants IBN-99-74927 and IBN-03-43127 to A.J.B.
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LITERATURE CITED |
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-
Aspinall D, Paleg LG. 1981. Proline accumulation: physiological aspects. In: Paleg LG, Aspinall D, eds. The physiology and biochemistry of drought resistance in plants. Sydney: Academic Press, 205–241.
Baluska F, Volkmann D, Barlow PW. 1996. Specialized zones of development in roots: view from the cellular level. Plant Physiology 112: 3–4.[Web of Science][Medline]
Bingham IJ, Blackwood JM, Stevenson EA. 1997. Site, scale and time-course for adjustments in lateral root initiation in wheat following changes in C and N supply. Annals of Botany 80: 97–106.
Bloom AJ. 1996. Nitrogen dynamics in plant growth systems. Life Support and Biosphere Sciences 3: 35–41.
Bloom AJ. 1997a. Interactions between inorganic nitrogen nutrition and root development. Zeitschrift für Pflanzennährung und Bodenkunde 160: 253–259.
Bloom AJ. 1997b. Nitrogen as a limiting factor: crop acquisition of ammonium and nitrate. In: Jackson LE, ed. Ecology in Agriculture. San Diego: Academic Press, 145–172.
Bloom AJ, Finazzo J. 1986. The influence of ammonium and chloride on potassium and nitrate absorption by barley roots depends on time of exposure and cultivar. Plant Physiology 81: 67–69.
Bloom AJ, Sukrapanna S. 1990. Effects of exposure to ammonium and transplant shock upon the induction of nitrate absorption. Plant Physiology 94: 85–90.
Bloom AJ, Jackson LE, Smart DR. 1993. Root growth as a function of ammonium and nitrate in the root zone. Plant, Cell and Environment 16: 199–206.
Bloom AJ, Meyerhoff PA, Taylor AR, Rost TL. 2002. Root development and absorption of ammonium and nitrate from the rhizosphere. Journal of Plant Growth Regulation 21: 416–431.[CrossRef]
Bloom AJ, Sukrapanna SS, Warner RL. 1992. Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiology 99: 1294–1301.
Boyer JS, Silk WK. 2004. Hydraulics of plant growth. Functional Plant Biology 31: 761–773.[CrossRef][Web of Science]
Bret-Harte MS, Silk WK. 1994a. Fluxes and deposition rates of solutes in growing roots of Zea mays. Journal of Experimental Botany 45: 1733–1742.[Web of Science]
Bret-Harte MS, Silk WK. 1994b. Nonvascular, symplasmic diffusion of sucrose cannot satisfy the carbon demands of growth in the primary root tip of Zea mays L. Plant Physiology 105: 19–33.[Abstract]
Büntemeyer K, Lüthen H, Böttger M. 1998. Auxin-induced changes in cell wall extensibility of maize roots. Planta 204: 515–519.[CrossRef][Web of Science]
Chazen O, Neumann PM. 1994. Hydraulic signals from the roots and rapid cell-wall hardening in crowing maize (Zea mays L.) leaves are primary responses to polyethylene glycol-induced water deficits. Plant Physiology 104: 1385–1392.[Abstract]
Chen R, Guan CH, Boonsirichai K, Masson PH. 2002. Complex physiological and molecular processes underlying root gravitropism. Plant Molecular Biology 49: 305–317.[Medline]
Cosgrove DJ. 1999. Enzymes and other agents that enhance cell wall extensibility. Annual Review of Plant Physiology and Plant Molecular Biology 50: 391–417.[CrossRef][Web of Science][Medline]
Deane-Drummond CE. 1986. A comparison of regulatory effects of chloride on nitrate uptake, and of nitrate on chloride uptake into Pisum sativum seedlings. Physiologia Plantarum 66: 115–121.
DeClerck F, Singer MJ. 2003. Looking back 60 years, California soils maintain overall chemical quality. California Agriculture 57: 38–41.
Drew MC. 1975. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75: 479–90.[CrossRef][Web of Science]
Edwards KL, Scott TK. 1974. Rapid growth responses of corn root segments: effect of pH on elongation. Planta 119: 27–37.[CrossRef]
Epstein E, Bloom AJ. 2005. Mineral Nutrition of Plants: Principles and Perspectives, 2nd edn. Sunderland, MA: Sinauer Associates.
Evans ML. 1976. A new sensitive root auxanometer. Plant Physiology 58: 599–601.
Forde BG. 2002. The role of long-distance signalling in plant responses to nitrate and other nutrients. Journal of Experimental Botany 53: 39–43.
Frensch J, Hsiao TC. 1994. Transient responses of cell turgor and growth of maize roots as affected by changes in water potential. Plant Physiology 104: 247–254.[Abstract]
Frensch J, Hsiao TC. 1995. Rapid response of the yield threshold and turgor regulation during adjustment of root growth to water stress in Zea mays. Plant Physiology 108: 303–312.[Abstract]
Frensch J, Steudle E. 1989. Axial and radial hydraulic resistance to roots of maize. Plant Physiology 91: 719–726.
Friml J. 2003. Auxin transport—shaping the plant. Current Opinion in Plant Biology 6: 7–12.[CrossRef][Web of Science][Medline]
Glass ADM, Thompson RG, Bordeleau L. 1985. Regulation of influx in barley: studies using 13. Plant Physiology 77: 379–381.
Gould N, Thorpe MR, Minchin PEH, Pritchard J, White PJ. 2004. Solute is imported to elongating root cells of barley as a pressure driven-flow of solution. Functional Plant Biology 31: 391–397.[CrossRef]
Goyal SS, Rains DW, Huffaker RC. 1988. Determination of ammonium ion by fluorometry or spectrophotometry after on-line derivatization with o-phthalaldehyde. Analytical Chemistry 60: 175–179.[Medline]
Grime JP, Crick JC, Rincon JE. 1986. The ecological significance of plasticity. In: Jennings DH, Trewavas AJ, eds. Plasticity in plants. Cambridge: Company of Biologists Limited; 5–29.
Hackett C. 1972. A method of applying nutrients locally to roots under controlled conditions, and some morphological effects of locally applied nitrate on the branching of wheat roots. Australian Journal of Biological Sciences 25: 1169–1180.
Jackson LE, Bloom AJ. 1990. Root distribution in relation to soil nitrogen availability in field-grown tomatoes. Plant Soil 128: 115–126.[CrossRef]
Kotake T, Nakagawa N, Takeda K, Sakurai N. 2000. Auxin-induced elongation growth and expressions of cell wall-bound exo- and endo-beta-glucanases in barley coleoptiles. Plant and Cell Physiology 41: 1272–1278.
Lockhart JA. 1965. An analysis of irreversible plant cell elongation. Journal of Theoretical Biology 8: 264–276.[CrossRef][Web of Science][Medline]
McIntyre GI. 2001. Control of plant development by limiting factors: a nutritional perspective. Physiologia Plantarum 113: 165–175.[CrossRef][Medline]
McLean EO, Brown JR. 1984. Crop response to lime in the midwestern United States. In: Adam F, ed. Soil acidity and liming. Madison, WI: ASA, CSSA, and SSSA.
Miller AL, Gow NAR. 1989. Correlation between root-generated ionic currents, pH, fusicoccin, indoleacetic-acid, and growth of the primary root of Zea mays. Plant Physiology 89: 1198–1206.
Neumann PM. 1993. Rapid and reversible modifications of extension capacity of cell-walls in elongating maize leaf tissues responding to root addition and removal of NaCl. Plant, Cell and Environment 16: 1107–1114.[CrossRef]
Peters WS. 2004. Growth rate gradients and extracellular pH in roots: how to control an explosion. New Phytologist 162: 571–574.[CrossRef]
Peters WS, Felle HH. 1999. The correlation of profiles of surface pH and elongation growth in maize roots. Plant Physiology 121: 905–912.
Peters WS, Luethen H, Boettger M, Felle H. 1998. The temporal correlation of changes in apoplast pH and growth rate in maize coleoptile segments. Australian Journal of Plant Physiology 25: 21–25.
Rayle DL, Cleland RE. 1992. The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiology 99: 1271–1274.
Rhodes D, Nadolska-Orczyk A, Rich PJ. 2002. Salinity, osmolytes and compatible solutes. In: Läuchli A, Lüttge U, eds. Salinity: environment–plants–molecules. Dordrecht: Kluwer Academic Publishers; 181–204.
Robinson D, Hodge A, Griffiths BS, Fitter AH. 1999. Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proceedings of the Royal Society of London, Series B 266: 431–435.
Sattelmacher B, Thoms K. 1989. Root growth and 14C-translocation into the roots of maize (Zea mays L.) as influenced by local nitrate supply. Zeitschrift für Pflanzennährung und Bodenkunde 152: 7–10.
Scherer HW, MacKnown CT, Leggett JE. 1984. Potassium–ammonium uptake interactions in tobacco seedlings. Journal of Experimental Botany 35: 1060–1070.
Schopfer P. 2001. Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. The Plant Journal 28: 679–688.[CrossRef][Web of Science][Medline]
Sharp RE, Hsiao TC, Silk WK. 1990. Growth of the maize primary root at low water potentials. 2. Role of growth and deposition of hexose and potassium in osmotic adjustment. Plant Physiology 93: 1337–1346.
Siebrecht S, Mack G, Tischner R. 1995. Function and contribution of the root tip in the induction of uptake along the barley root axis. Journal of Experimental Botany 46: 1669–1676.
Smart DR, Bloom AJ. 1988. Kinetics of ammonium and nitrate uptake among wild and cultivated tomatoes. Oecologia 76: 336–340.[CrossRef]
Smart DR, Bloom AJ. 1998. Investigations of ion absorption during exposure. I. Relationship between H+ efflux and absorption. Journal of Experimental Botany 49: 95–100.
Snir N, Neumann PM. 1997. Mineral nutrient supply, cell wall adjustment and the control of leaf growth. Plant, Cell and Environment 20: 239–246.[CrossRef]
Tanimoto E, Fujii S, Yamamoto R, Inanaga S. 2000. Measurement of viscoelastic properties of root cell walls affected by low pH in lateral roots of Pisum sativum L. Plant and Soil 226: 21–28.[CrossRef]
Taylor AR, Bloom AJ. 1998. Ammonium, nitrate, and proton fluxes along the maize root. Plant, Cell and Environment 21: 1255–1263.[CrossRef]
Thayer JR, Huffaker RC. 1980. Determination of nitrate and nitrite by High-Pressure Liquid Chromatography: comparison with other methods for nitrate determination. Analytical Biochemistry 102: 110–119.[CrossRef][Web of Science][Medline]
Van Volkenburgh E. 1999. Leaf expansion—an integrating plant behaviour. Plant, Cell and Environment 22: 1463–1473.[CrossRef]
Walter A, Silk WK, Schurr U. 2000. Effect of soil pH on growth and cation deposition in the root tip of Zea mays L. Journal of Plant Growth Regulation 19: 65–76.[Medline]
Walter A, Feil R, Schurr U. 2003. Expansion dynamics, metabolite composition and substance transfer of the primary root growth zone of Zea mays L. grown in different external nutrient availabilities. Plant, Cell and Environment 26: 1451–1466.[CrossRef]
Weisenseel MH, Dorn A, Jaffe LF. 1979. Natural H+ currents traverse growing roots and root hairs of barley (Hordeum vulgare L.). Plant Physiology 64: 512–518.
Winch S, Pritchard J. 1999. Acid-induced wall loosening is confined to the accelerating region of the root growing zone. Journal of Experimental Botany 50: 1481–1487.
Wu Y, Sharp RE, Durachko DM, Cosgrove DJ. 1996. Growth maintenance of the maize primary root at low water potentials involves increases in cell-wall extension properties, expansion activity, and wall susceptibility to expansions. Plant Physiology 111: 765–772.[Abstract]
Zhang HM, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the USA 96: 6529–6534.
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  T. L. Rost and A. J. Bloom Preface. Ann. Bot., May 1, 2006; 97(5): 837 - 838. [Full Text] [PDF]
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