HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (12) Citing Articles via Google Scholar Google Scholar Articles by Ferrufino, A. Articles by Carter, T. E. Search for Related Content PubMed Articles by Ferrufino, A. Articles by Carter, T. E., Jr. Agricola Articles by Ferrufino, A. Articles by Carter, T. E.

CROP PHYSIOLOGY & METABOLISM

Root Elongation of Soybean Genotypes in Response to Acidity Constraints in a Subsurface Solution Compartment

^a Programa de Apoyo a la Estrategia de Desarollo Alternativo (PRAEDAC), P.O. Box 2395, Cochabamba, Bolivia
^b USDA-ARS Soil Science Dep., North Carolina State University, Raleigh, NC 27695-7619 USA
^c USDA-ARS Crop Science Dep., North Carolina State University, Raleigh, NC 27695-7620 USA

jot_smyth{at}ncsu.edu

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Aluminum-tolerant germplasm is needed to overcome subsurface acidity constraints to root growth and plant access to water and nutrients. Root elongation of four soybean [Glycine max (L.) Merr.] genotypes exposed to varying concentrations of Al, H, and Ca were compared in two experiments using a vertically split root system. Roots extending from a limed surface soil compartment grew for 12 d into a subsurface compartment with nutrient solution treatments. In Exp. 1 root growth for cv. Ransom and Plant Introduction 416937 (PI) were compared in solutions with factorial combinations of pH (4.2, 5.2) and Al (0, 7.5, 15 µM) with Ca maintained at 10 mM. In Exp. 2 soybean line N93-S-179 (N93), PI, and cultivars Ransom and Young were compared in solutions with factorial combinations of Ca (2 and 10 mM) and Al (7.5 and 15 µM) maintained at pH 4.6. Ransom and PI had similar responses in tap and lateral root elongation to solution pH and Al treatments in Exp. 1, but mean tap root length of Ransom in the subsurface compartment exceeded that of PI by 22%. Aluminum inhibited the length of lateral roots more than tap roots in both experiments. Molar activity ratios between Ca and Al³⁺ {Ca/Al³⁺} accounted for most of the differences in root elongation response among solution treatments in Exp. 2. A 50% reduction in relative length of tap roots for all genotypes occurred with a {Ca/Al³⁺} value of 891. Values of {Ca/Al³⁺} for 50% reductions in relative length of lateral roots differed among genotypes and were 1.6 to 3.5 times greater than for tap roots. On the basis of the {Ca/Al³⁺} indices for lateral root length, line N93 and Ransom exhibited greater tolerance to subsurface solution Al than PI and Young.

Abbreviations: Al_a, fraction of Al in solution that reacts immediately with the ferron reagent • Al_b, fraction of Al in solution that reacts with ferron according to first order kinetics • Al_T, all Al in solution that reacts with ferron • AlFN₃₀, Al in solution reacting with ferron by 30 s • Al_Mono, Al³⁺ + Al²⁺ + Al⁺₂ + Al⁰₃ + Al^-₄ • {Ca/Al³⁺}, molar activity ratio between Ca and trivalent Al • N93, breeding line N93-S-179 • PI, Plant Introduction 416937

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
DEVELOPMENT OF SOYBEAN ROOTS in acid soils is restricted by low pH, low contents of Ca and Mg, and high Al (Goldman et al., 1989; Carter and Rufty, 1993; Spehar, 1994). Liming alleviates constraints of soil acidity in surface layers (Dierolf et al., 1997), but subsurface layers may remain acid and can have low Ca concentrations (Ritchey et al., 1980). Subsoil acidity reduces crop yields by restricting root growth and thereby reducing nutrient acquisition and plant access to soil water reserves during periods of drought stress. Potential alternatives to the direct amelioration of subsoil acidity include the use of Al-tolerant germplasm (Foy, 1988).

Aluminum rhizotoxicity for several plant species can be alleviated by increasing the Ca concentration in nutrient solutions (Alva et al., 1986a, 1986b; Horst, 1987; Runge and Rode, 1991). Calcium additions alleviate Al rhizotoxicity by reducing Al activity through increased solution ionic strength and increased competition between Ca and Al at binding sites external to the plasmalema (Kinraide and Parker, 1987). Other roles for Ca include increasing membrane hydrophobicity; preventing cell leakiness; strengthened cell walls; and, in the cytoplasm, acting as a "second messenger" that mediates changes in enzyme activity (Hanson, 1984; Marschner, 1995).

Different classes of roots for the same genotype can exhibit differential elongation responses to rhizotoxic Al. Bushamuka and Zobel (1998), in a comparison of elongation of tap, basal, and lateral roots between limed and unlimed subsurface layers of Al-toxic soil among several maize (Zea mays L.) and soybean cultivars, found that tolerance to Al in the unlimed subsurface layer by all three root classes was only observed in one maize cultivar. However, among the other maize and soybean cultivars, either one, two, or none of these root classes were tolerant to the soil Al stress. Sanzonowicz et al. (1998a, 1998b) found that subsurface solution H and Al inhibited the length of lateral roots more than tap roots for Ransom soybean. When exposed to similar levels of toxic H or Al, a higher solution Ca concentration was needed to increase length of lateral roots relative to tap roots.

The objective of this investigation was to compare root elongation response to varying solution concentrations of H and Al and the ameliorative effects of Ca among different classes of roots for selected soybean genotypes exposed to rhizotoxic treatments in the subsurface compartment of a vertically split root system.

	Materials and methods

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
A vertically split root system (Sanzonowicz et al., 1998a) was used to evaluate elongation of soybean roots extending from a limed surface soil into a subsurface zone containing solutions with various combinations of Al, pH, and Ca. Plastic tubes, 52 cm long with an internal diameter of 10 cm, were divided into two sections separated by a root-permeable membrane. The membrane was formed by dipping cheesecloth attached to the surface compartment into a mixture of paraffin and petrolatum (1:2) at 80°C for 10 s. Both tube sections were disinfected with 20.6 M ethanol.

The 12-cm-long surface compartment was filled with 1.1 kg of sterilized (121°C, 0.1 MPa for 1 h) loamy sand from the Ap horizon of a Wagram soil (loamy, kaolinitic, thermic Arenic Kandiudult). Selected chemical properties of this soil are described elsewhere (Sanzonowicz et al., 1998a). The soil was limed to pH 5.5 with CaCO₃ and received 30 mg K kg^-1 as KCl before sterilization. The subsurface compartment, which was used for treatment solutions, contained 3.0 L of solution continuously aerated with air prefiltered through a high efficiency particulate filter. Solutions in all experiments contained 18.5 µM B as H₃BO₃ and 0.5 µM Zn as ZnCl₂, since root elongation of Ransom decreased in the subsurface compartment when these nutrients were omitted (Sanzonowicz et al., 1998a). Aluminum was supplied as AlCl₃ from a 0.037 M acidified stock solution and Ca as CaCl₂. Solution pH was adjusted daily by titration with 0.05 M solutions of either HCl or NaOH. Solutions were replaced every 4 d.

Experiment 1 was conducted during October in a greenhouse at North Carolina State University in Raleigh, NC. Natural light was supplemented by 150 µmol m^-2 s^-1 of photosynthetically active radiation from metal halide lamps for 16 h d^-1. Treatments in the subsurface solution compartment consisted of a factorial combination of three Al concentrations (0, 7.5, and 15 µM) and two pH levels (4.2 and 5.2) with a constant supply of Ca (10 mM). Root elongation into these subsurface solution treatments was compared between soybean plant introduction 416937 (PI), which is part of the USDA plant germplasm collection, and Ransom (Brim and Elledge, 1973).

Experiment 2 was conducted in a walk-in chamber of the phytotron at North Carolina State University (Thomas and Downs, 1991) with day/night temperatures of 26/22°C, 70% relative humidity, and a 12-h photoperiod. Light was provided by incandescent and fluorescent lamps at a photosynthetic photon flux density of 639 mol m^-2 s^-1. Treatments in the subsurface solution compartment consisted of a factorial combination of two Al concentrations (7.5 and 15 µM) and two Ca concentrations (2 and 10 mM) maintained at pH 4.6. Root elongation into these solution treatments was compared among four soybean genotypes: PI, Ransom, Young (Burton et al., 1987), and breeding line N93-S-179 (N93). Breeding line N93 was selected by USDA-ARS at North Carolina State University from a cross of Young and PI. Treatments were arranged in a randomized complete block design with three replications.

Seeds for both experiments were surface-sterilized with ethanol for 1 min and 26.9 mM sodium hypochlorite for 3 min, rinsed six times with sterile water (Ramirez et al., 1997), and placed in the dark at 28°C in paper towels moistened with sterile 500 µM CaSO₄ to germinate. Five seedlings of each genotype with a tap root length of 3 ± 0.5 cm were planted in the upper compartment and thinned to four plants after 3 d. Soil moisture content was adjusted daily to 80% of container capacity (Cassel and Nielsen, 1986).

For both experiments tap root length in the subsurface compartment was measured daily. Among roots extending through the membrane, lateral and basal classes (Zobel, 1991) could not be distinguished and were combined into a group designated as "other" roots. Microbial contamination was minimized by disinfecting all tools with 20.6 M ethanol and by using sterilized distilled water in the subsurface compartment.

Plants were harvested 13 d after planting, which coincided with natural abscission of cotyledons and emergence of the second trifoliolate leaf. Plant shoots were dried at 55°C for 2 d, weighed, ground, dry ashed at 500°C, dissolved in 0.5 M HCl, and analyzed for Al and Ca by atomic absorption spectrophotometry.

Tap roots, their lateral roots, and "other" roots in the hydroponic solutions were separated at harvest and counted. Roots were refrigerated in 4.3 M ethanol until their length could be measured by edge discrimination (Pan and Bolton, 1991) using a desktop scanner preset to a resolution of 98 dots cm^-1 (250 dots per inch). Roots in the soil compartment were washed free of soil and their combined total length was measured following the same procedure. Relative root length for a root class within an experiment was calculated as the ratio between a given treatment and the treatment with the greatest length.

Aluminum reacting with ferron (Bersillon et al., 1980) was measured in solution aliquots collected at Day 12 from all treatments in both experiments that contained Al. The ferron reagent was mixed with sample aliquots at a sample/reagent volume ratio of 1:3 through forced-injection into a cuvette, and absorbance readings were recorded with an automatic chart recorder from within 1 s of reagent addition until negligible changes in absorbance were observed. Matrix effects observed on ferron readings due to different Ca concentrations in solutions for Exp. 2 were taken into account by using separate standard curves for each Ca level. Two different fractions of Al, Al_a and Al_b, were characterized in the solutions using the procedure of Smith (1971). The Al_a fraction includes monomeric Al species that react almost immediately with ferron, and the Al_b fraction contains metastable Al polymers that react with ferron according to first-order kinetics. Total ferron-reactive Al (Al_T) was estimated by the following equation (Jallah and Smyth, 1998):

where Al_ab is the maximum value of reactive Al within the reaction time, Al⁰_a is Al_a at zero time (t), and K_b is the rate of reaction of Al_b. Nonlinear regression procedures (SAS Institute, 1985) were used to calculate Al_a, Al_b, and Al_ab. The GEOCHEM-PC program (Parker et al., 1995) was used to predict Al speciation in the different solution treatments.

Statistical analysis of variables measured over time was performed with a split-plot model, with the factorial combination of genotypes, Al, and pH levels as main plots, and time as the subplot. Variables measured at harvest were analyzed as a complete factorial in a randomized complete block design.

	Results and discussion

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Solution Aluminum Characteristics among Experiments and Treatments
Solution treatments in the subsurface compartment of both experiments affected Al speciation and ferron-reactive Al fractions (Table 1) . Trivalent Al was the predominant monomeric Al species in solutions maintained at pH 4.2 and 4.6, whereas hydroxy-Al species were dominant in solutions maintained at pH 5.2. Increasing Ca concentration in solutions from 2 to 10 mM for Exp. 2 increased ionic strength and Ca activity and decreased the GEOCHEM-predicted activity of the sum of monomeric Al by 50%. Previous investigators have used the Al reacting with ferron by 30 s (AlFN₃₀) as an index of inorganic monomeric Al (Jardine and Zelazny, 1987; Wright et al., 1987). In solutions for both of our experiments trivalent Al activity correlated with the Al_a (r = 0.73, P < 0.05), Al_b (r = 0.77, P < 0.05) and ALFN₃₀ (r = 0.83, P < 0.01) fractions, but neither the predicted activities of individual hydroxy-Al species nor the sum of monomeric Al species was significantly correlated with these ferron-reactive Al fractions.

Experiment 1
Tap Root Elongation
Tap root elongation in the subsurface solution compartment followed a curvilinear trend, but there were no significant differences (P < 0.05) in genotypic response to pH and Al treatments (data not shown). When averaged across pH and Al levels, tap root length for Ransom was greater than for PI (P < 0.01) throughout the final 6 d of growth. At harvest, tap root length for Ransom exceeded that for PI by 22%. A significant interaction (P < 0.01) between Al and pH revealed that tap root length, averaged across genotypes, decreased with increasing Al levels at pH 4.2 (Fig. 1) . In solutions maintained at pH 5.2 there was no difference in tap root elongation between 0 and 7.5 µM Al treatments, whereas root elongation stopped after Day 9 when exposed to 15 µM Al. Less inhibition of tap root elongation by 15 µM Al at pH 4.2 than at 5.2 may be related to the relief of Al³⁺ toxicity by increases in H⁺, as recently proposed by Kinraide (1997), but Al solutions at pH 5.2 also presented conditions favorable to the formation of the rhizotoxic triskaidekaaluminium (Al₁₃) species (Kinraide, 1997). Sanzonowicz et al. (1998a) reported similar interactions between pH and Al on tap root length for Ransom in a vertically split–root experiment containing a broader range of subsurface solution treatments (pH 4.0–5.2 and 0–30 µM Al).

View larger version (17K): [in this window] [in a new window]   Fig. 1 Mean soybean tap root length as a function of time in subsurface solution Al treatments maintained at pH values of (a) 4.2 and (b) 5.2 in Exp. 1. Symbols are observed values averaged across genotypes Ransom and PI, and lines are predicted values from polynomial regression models. Vertical bar denotes least significant difference (P < 0.05) for the pH by Al by time interaction

The combined length of all root classes in the solution compartment at harvest was significantly greater (P < 0.01) for Ransom than for PI. Total root length for Ransom exceeded that of PI by 22% when averaged across Al and pH treatments. Although there were no differences in genotypic response to solution Al and pH treatments, reductions in total root length with increasing solution Al concentration differed between solutions at pH 4.2 and 5.2, when averaged across genotypes (Fig. 2) . Inhibition of total root length by the 7.5 µM Al treatment was greater in solutions maintained at pH 4.2 than at 5.2, whereas inhibition of root length with 15 µM Al was similar at both pH levels.

View larger version (33K): [in this window] [in a new window]   Fig. 2 Total soybean root length and length of individual root classes at harvest in subsurface solution pH and Al treatments in Exp. 1. Root length is averaged across genotypes Ransom and PI. Vertical bar denotes the least significant difference (P < 0.05) for total root length

In separate experiments comparing tap root elongation among soybean genotypes upon exposure to Al in single-compartment hydroponic systems, investigators ranked PI as Al-tolerant (Villagarcia et al., 1997) and Ransom as Al-sensitive (Sartain and Kamprath, 1978). However, neither of these investigations contained both genotypes. Although our direct comparisons of these genotypes in a vertically split–root system revealed that PI had greater root length in the limed soil compartment, there were no differences in genotypic responses to Al and H⁺ inhibition of either the combined or individual elongation of several root classes in the subsurface solution compartment.

Experiment 2
Tap Root Length and Characteristics of Laterals and Other Roots at Harvest
During 12 d of exposure to subsurface solution Al and Ca treatments, tap root elongation of soybean genotypes N93, PI, Ransom, and Young followed curvilinear trends similar to those shown in Fig. 1 for PI and Ransom in Exp. 1 (data not shown). Likewise, differences in tap root elongation among genotypes to solution treatments were reflected in root length measurements taken at harvest. Tap root length at harvest was significantly different (P < 0.05) among genotypes when averaged across solution Al and Ca treatments. Genotypic ranking for tap root length was: Ransom > Young > N93 = PI (Table 4) . When comparing main effects of solution Al and Ca treatments, tap root length decreased by 34% between 7.5 and 15 µM Al and increased by threefold between 2 and 10 mM Ca. Inhibition of tap root length by Al among genotypes was influenced by the solution Ca concentration. Tap root length with 2 mM Ca, averaged across Al treatments, was similar among genotypes (mean of 27 cm per pot), but tap root length for cultivars Ransom and Young was greater than for line N93 and PI when solutions contained 10 mM Ca. These genotypic differences in tap root elongation for Al treatments with 10 mM Ca were only evident after 9 d of root exposure to the subsurface solutions (data not shown). Relief of Al inhibition of soybean tap root elongation upon increasing solution Ca concentration has been reported for several genotypes in experiments with both single-compartment (Alva et al., 1986b; Noble et al., 1988) and vertically split–root systems (Lund, 1970; Sanzonowicz et al., 1998b).

View larger version (25K): [in this window] [in a new window]   Fig. 3 Number of lateral roots on tap roots at harvest in the subsurface compartment for soybean genotypes N93 (N), Ransom (R), PI, and Young (Y), as a function of Al concentration in solutions with 2 and 10 mM Ca in Exp. 2. Vertical bar denotes the least significant difference (P < 0.05) for the genotype x Al x Ca interaction

Total Root Length at Harvest
Genotypic differences in the combined length of tap, lateral, and other roots in the subsurface solution compartment depended on the solution Al and Ca treatments (Fig. 4) . In solutions containing 2 mM Ca, total root length of soybean genotypes was similar between treatments containing either 7.5 or 15 µM Al. Increasing Al concentration in solutions with 10 mM Ca decreased total root length by 56% for PI and 61% for Young, but there was no significant change for line N93 and Ransom. Genotypic ranking for total root length in solutions with 10 mM Ca also differed between Al treatments. At 7.5 µM Al total root length of Young was greater than for line N93 and PI; whereas at 15 µM Al total root length for Ransom was greater than that of PI and Young. Among the different root classes, the greatest reduction in length in response to increased Al stress at 10 mM Ca occurred with lateral roots; between 7.5 and 15 µM Al, reductions in length of root classes averaged across genotypes were 63% for lateral roots, 26% for tap roots, and 33% for other roots.

View larger version (27K): [in this window] [in a new window]   Fig. 4 Total root length at harvest as a function of root classes and solution Al and Ca treatments in the subsurface compartment for soybean genotypes N93 (N), Ransom (R), PI, and Young (Y) in Exp. 2. Vertical bar denotes least significant difference (P < 0.05) for the genotype x Al x Ca interaction

View larger version (18K): [in this window] [in a new window]   Fig. 5 Observed (symbols) and predicted (lines) relative length at harvest of (a) tap roots and (b) lateral roots of soybean genotypes N93, Ransom, PI, and Young in the subsurface solution compartment as a function of the molar activity ratios between Ca and Al3+ in Exp. 2. Prediction equations are shown in Table 8

	Conclusions

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
By simulating acidity conditions underlying a limed surface soil, the vertically split–root system used in these experiments allows assessment of root elongation responses to H⁺, Al, and Ca with minimum confounding effects on shoot growth. The only difference in tap root elongation among genotypes to subsurface solution treatments was for the mean value across Al treatments with 10 mM Ca; lengths for Ransom and Young were greater than for line N93 and PI. However, in both experiments, mean values of tap root length averaged across solution treatments for Ransom were greater than for the other genotypes tested.

Hydrogen and Al inhibited the length of lateral roots to a greater extent than tap roots. Alleviation of the inhibitory effect of Al on root length by increasing Ca supply in solutions also required greater Ca concentrations for laterals than for tap roots. Expression of genotypic differences in lateral root length to rhizotoxic Al was influenced by the associated level of Ca supplied in the solutions. On the basis of the relative length of lateral roots across solutions with varying molar activity ratios between Ca and Al³⁺, Ransom and line N93 had greater tolerance rankings than Young and PI. Based on the absolute total length of roots in the subsurface compartment, similar genotypic rankings for Al tolerance were obtained in the treatment with 15 µM Al and 10 mM Ca; total root length for Ransom was similar to line N93 and greater than that for PI and Young. The observed differences among genotypes in tap and lateral root length upon exposure to solution Al illustrate the importance of characterizing individual root classes when screening soybean germplasm for Al tolerance.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Research supported by the Soil Management Collaborative Research Support Program and funded in part by Grant no. DAN-1311-G-00-1049-00 from the USAID.

Received for publication February 5, 1999.

	REFERENCES

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 

• Alva A.K., Asher C.J., Edwards D.G. The role of calcium in alleviating aluminium toxicity. Aust. J. Agric. Res. 1986;37:375-382 a.
• Alva A.K., Edwards D.G., Asher C.J., Blamey F.P.C. Effects of phosphorus/aluminum molar ratio and calcium concentration on plant response to aluminum toxicity. Soil Sci. Soc. Am. J. 1986;50:133-137 b.[Abstract/Free Full Text]
• Bersillon J.L., Hsu P.H., Fiessinger F. Characterization of hydroxy aluminum solutions. Soil Sci. Soc. Am. J. 1980;44:630-634.[Abstract/Free Full Text]
• Brim C.A., Elledge C. Registration of Ransom soybean. Crop Sci. 1973;13:130.[Free Full Text]
• Burton J.W., Brim C.A., Young M.F. Registration of `Young' soybean. Crop Sci. 1987;27:1093.[Free Full Text]
• Bushamuka V.N., Zobel R.W. Maize and soybean tap, basal, and lateral root responses to a stratified acid, aluminum-toxic soil. Crop Sci. 1998;38:416-421.[Abstract/Free Full Text]
• Carter T.E., Jr., Rufty T.W. Soybean plants introductions exhibiting drought and aluminum tolerance. In: Kuo C.G., ed. Adaptation of food crops to temperature and water stress: proceedings of an international symposium. Tapei, Taiwan: Taiwan. 13–18 Aug. 1992. Publ. no. 93-410. Asian Vegetable Research and Development Center, 1993:335-346.
• Cassel D.K., Nielsen D.R. Field capacity and available water capacity. In: Kutle A., ed. Methods of soil analysis, Part 1, 2nd ed Madison, WI: ASA and SSSA, 1986:901-926 Agron. Monogr. 9.
• Dierolf T.S., Arya L.M., Yost R.S. Water and cation movement in an Indonesian ultisol. Agron. J. 1997;89:572-579.[Abstract/Free Full Text]
• Foy C.D. Plant adaptation to acid, aluminum-toxic soils. Commun. Soil Sci. Plant Anal. 1988;19:959-987.
• Goldman I.L., Carter T.E., Jr., Patterson R.P. Differential genotypic response to drought stress and subsoil aluminum in soybean. Crop Sci. 1989;29:330-334.
• Hanson J.B. The functions of calcium in plant nutrition. In: Tinker P.B., Lauchli A., eds. Advances in plant nutrition. Vol. 1. New York: Preager, 1984:149-208.
• Horst W.J. Aluminium tolerance and calcium efficiency of cowpea genotypes. J. Plant Nutr. 1987;10:1121-1129.
• Hudak C.M., Patterson R.P. Vegetative growth analysis of a drought-resistant soybean plant introduction. Crop Sci. 1995;35:464-471.[Abstract/Free Full Text]
• Jallah J.K., Smyth T.J. Assessment of rhizotoxic aluminum in soil solutions by computer and chromogenic speciation. Commun. Soil Sci. Plant Anal. 1998;29:37-50.
• Jardine P.M., Zelazny L.W. Influence of organic anions on the speciation of mononuclear and polynuclear aluminum by ferron. Soil Sci. Soc. Am. J. 1987;51:885-889.[Abstract/Free Full Text]
• Kinraide T.B. Reconsidering the rhizotoxicity of hydroxyl, sulphate, and fluoride complexes of aluminium. J. Exp. Bot. 1997;48:1115-1124.
• Kinraide T.B., Parker D.R. Cation amelioration of aluminum toxicity in wheat. Plant Phys. 1987;84:546-551.
• Kinraide T.B., Ryan P.R., Kochian L.V. Al³⁺–Ca²⁺ interactions in aluminum rhizotoxicity. Planta 1994;192:104-109.[ISI]
• Lund Z.F. The effect of calcium and its relation to several cations in soybean root growth. Soil Sci. Soc. Am. Proc. 1970;34:456-459.
• Marschner H. Mineral nutrition of higher plants, 2nd ed New York: Academic Press, 1995.
• Noble A.D., Fey M.V., Sumner M.E. Calcium–aluminum balance and the growth of soybean roots in nutrient solutions. Soil Sci. Soc. Am. J. 1988;52:1651-1656.[Abstract/Free Full Text]
• Pan W.L., Bolton R.P. Root quantification by edge discrimination using a desktop scanner. Agron. J. 1991;83:1047-1052.[Abstract/Free Full Text]
• Pantalone V.R., Rebetzke G.J., Burton J.W., Carter T.E., Jr. Phenotypic evaluation of root traits in soybean and applicability to plant breeding. Crop Sci. 1996;36:456-459.[Abstract/Free Full Text]
• Parker D.R., Norvell W.A., Chaney R.L. GEOCHEM-PC a chemical speciation program for IBM and compatible personal computers. In: Loeppert R.H., et al. , ed. Chemical equilibrium and reaction models. Madison, Wl: SSSA and ASA, 1995:253-269 SSSA Spec. Publ. 42..
• Ramirez M.E., Israel Daniel W., Wollum A.G. Phenotypic characterization of soybean Bradyrhizobia in two soils of North Carolina. Soil Biol. Biochem. 1997;29:1547-1555.
• Rengel Z. Role of calcium in aluminium toxicity. New Phytol. 1992;121:499-513.
• Ritchey K.D., Souza D.M.G., Lobato E., Correa O. Calcium leaching to increase rooting depth in a Brazilian savannah Oxisol. Agron. J. 1980;72:40-44.[Abstract/Free Full Text]
• Runge M., Rode M.W. Effects of soil acidity on plant associations. In: Ulrich B., Sumner M.E., eds. Soil acidity. Berlin: Springer, 1991:183-202.
• Sanzonowicz C., Smyth T.J., Israel D.W. Hydrogen and aluminum inhibition of soybean root extension from limed soil into acid subsurface solutions. J. Plant Nutr. 1998;21:387-403 a.
• Sanzonowicz C., Smyth T.J., Israel D.W. Calcium alleviation of hydrogen and aluminum inhibition of soybean root extension from limed soil into acid subsurface solutions. J. Plant Nutr. 1998;21:785-804 b.
• SAS Institute. SAS user's guide: Statistics, 5th ed Cary, NC: SAS Inst, 1985.
• Sartain J.B., Kamprath E.J. Aluminum-tolerance in soybean cultivars based on root elongation in solution culture compared with growth in acid soil. Agron. J. 1978;70:17-20.
• Sloane R.J., Patterson R.P., Carter T.E., Jr. Field drought tolerance of a soybean plant introduction. Crop Sci. 1990;30:118-123.[Abstract/Free Full Text]
• Smith R.W. Relations among equilibrium and non-equilibrium aqueous species of aluminum hydroxyl complexes. Am. Chem. Soc. Adv. Chem. 1971;106:250-279.
• Spehar C.R. Field screening of soya bean (Glycine max (L.) Merril) germplasm for aluminium tolerance by the use of augmented design. Euphytica 1994;76:203-213.
• Thomas, J.F., and R.J. Downs. 1991. Phytotron procedural manual for controlled-environment research at the Southeastern Plant Environment Laboratory. N.C. Agric. Res. Serv. Tech. Bull. 244, North Carolina State Univ., Raleigh.
• Villagarcia, M.R., T.E. Carter, Jr., T.W. Rufty, M.W. Jennette, C. Arellano, and C.M. Bianchi-Hall. 1997. Deferential aluminum tolerance in the genetic base of north American public soybean cultivars detected by hydroponic assay. p. 158. In Agron. Abstracts. ASA, Madison, WI.
• Wright R.J., Baligar V.C., Wright S.F. Estimation of phytotoxic aluminum in soil solution using three spectrophotometric methods. Soil Sci. 1987;144:224-232.
• Zobel R.W. Root growth and development. In: Keister D.L., Kregan P.B., eds. The rhizosphere and plant growth. Dordrecht, the Netherlands: Kluwer Academic Publ, 1991:61-71.

This article has been cited by other articles:

				H. Liao, H. Wan, J. Shaff, X. Wang, X. Yan, and L. V. Kochian Phosphorus and Aluminum Interactions in Soybean in Relation to Aluminum Tolerance. Exudation of Specific Organic Acids from Different Regions of the Intact Root System Plant Physiology, June 1, 2006; 141(2): 674 - 684. [Abstract] [Full Text] [PDF]

				P. W. Voigt and T. E. Staley Selection for Aluminum and Acid-Soil Resistance in White Clover Crop Sci., January 1, 2004; 44(1): 38 - 48. [Abstract] [Full Text] [PDF]

				M. R. Villagarcia, T. E. Carter Jr., T. W. Rufty, A. S. Niewoehner, M. W. Jennette, and C. Arrellano Genotypic Rankings for Aluminum Tolerance of Soybean Roots Grown in Hydroponics and Sand Culture Crop Sci., September 1, 2001; 41(5): 1499 - 1507. [Abstract] [Full Text] [PDF]

				I. R. Silva, T. J. Smyth, D. W. Israel, C. D. Raper, and T. W. Rufty Magnesium is More Efficient than Calcium in Alleviating Aluminum Rhizotoxicity in Soybean and its Ameliorative Effect is not Explained by the Gouy-Chapman-Stern Model Plant Cell Physiol., May 1, 2001; 42(5): 538 - 545. [Abstract] [Full Text] [PDF]

				I. R. Silva, T. J. Smyth, D. W. Israel, C. D. Raper, and T. W. Rufty Magnesium Ameliorates Aluminum Rhizotoxicity in Soybean by Increasing Citric Acid Production and Exudation by Roots Plant Cell Physiol., May 1, 2001; 42(5): 546 - 554. [Abstract] [Full Text] [PDF]

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (12) Citing Articles via Google Scholar Google Scholar Articles by Ferrufino, A. Articles by Carter, T. E. Search for Related Content PubMed Articles by Ferrufino, A. Articles by Carter, T. E., Jr. Agricola Articles by Ferrufino, A. Articles by Carter, T. E.