Environ. Sci. Technol. 2005, 39, 5247-5254
Calcium-(Organo)aluminum-proton Competition for Adsorption to Tomato Root Cell Walls: Experimental Data and Exchange Model Calculations JACQUELINE W. M. POSTMA,* WILLEM G. KELTJENS, AND WILLEM H. VAN RIEMSDIJK Soil Quality, Environmental Sciences, Wageningen University, P.O. Box 8005, 6700 EC Wageningen, The Netherlands
Aluminum interacts with negatively charged surfaces in plant roots, causing inhibition of growth and nutrient uptake in plants growing on acid soils. Pectins in the root cell wall form the major cation adsorption surface, with Ca2+ as the main adsorbing cation. Adsorption of Al3+ and Ca2+ to isolated cell wall material of tomato (Lycopersicon esculentum L.) roots was examined at pH 3.00-4.25 and in the presence of the aluminum chelators citrate and malate. Al3+ displaced Ca2+ from its pectic binding sites in the cell wall to a large extent but apparently also bound to nonCa binding groups, displacing protons. Aluminum adsorption depended on the pH of the solution, with little Al adsorbing to the cell wall material at very low pH ( 50 µM (Figure 1). A lower pH affected Ca adsorption in the absence of Al: incubating the cell wall material at pH 3.50 instead of 4.00 decreased [Ca]cw by approximately 30%. With added Al and especially at the higher Al concentrations, this pH effect disappeared, which is in marked contrast to the Al adsorption (Figure 1). With [Al]sol ) 100 µM and the pH range extended to 3.004.25, only little Al adsorbed at the lower end of the range but Al adsorption increased with increasing pH (Figure 2A). This was in agreement with the pH effect on Al adsorption found in the first experiment. A first-order regression model was used for a first approximation of the increase in Al adsorption with increasing pH. Ca adsorption, in the absence of Al, depended similarly on pH (Figure 2B). When 100 µM Al was
FIGURE 1. Al (diamonds) and Ca (squares) adsorption to isolated root cell wall material in relation to Al3+ activity ({Al3+}sol) and pH in the solution. Open and closed symbols represent pH 4.00 and 3.50, respectively (experiment 1). Bars indicate the standard deviation of the mean values. present, the [Ca]cw remained at 40-60 µmol (g DCW)-1 and was apparently not affected by either pH changes or changes in [Al]cw. This response was similar to the leveling off of Ca adsorption at higher Al activity in Figure 1. When [Al]cw was plotted against [Ca]cw, values were linearly correlated, with correlation coefficients of -0.98 and -0.99 for pH 3.50 and 4.00, respectively (Figure 3). Though total adsorption was distinctly lower at pH 3.50, compared to that at pH 4.00, the slopes of the two lines were the same, which related to an Al/Ca molar exchange ratio of 1:0.9 at both pH levels (Figure 3). Using part of the same pH range as in experiment 2 and comparing adsorption of Al in the presence of citrate with that of AlCl3, citrate addition decreased [Al]cw by 63% at pH 3.50 to 94% at pH 4.25 (Figure 2A). Ca adsorption, under these conditions, reached values of 85 and 94% of control [Ca]cw levels (Figure 2B). Citrate was most effective in preventing Al adsorption at the highest pH, when the organic acid was relatively more deprotonated. The decrease in Al adsorption could also be recognized in the slightly steeper slope of Ca adsorption: the less Al adsorbed to the cell wall, the more Ca adsorption approached its control (-Al) level. Performing the experiment at pH 3.50 and 4.00 with 100 µM Al-malate instead of Al-citrate resulted in a limited prevention of Al adsorption: malate decreased [Al]cw by 16% (pH 3.50) and 37% (pH 4.00) (Figure 2A). The marginal improvement of [Ca]cw compared to the Al treatment without organic anions was consistent with a still high [Al]cw (Figure 2B). Gaines-Thomas Exchange Model Simulations. For a first estimation of exchange coefficients for Ca\H and Al\H, the intersects of the trend line for pH 3.50 with the x- and y-axes in Figure 3 were taken as the adsorption of Ca at [Al]sol ) 0 and of Al at [Ca]sol ) 0, respectively. Multiplying these values with their valencies gave the adsorption in meq (g DCW)-1. For an approximation of the cation activity in the solution, an average of the calculated activity values was taken for all samples at pH 3.50, providing the input and KGT values, calculated according to eqs 2, 4, and 8 (Table 3). Using these values of KGTAl\Ca and KGTH\Ca () (KGTCa\H)-1), with Ca2+ as the reference ion, provided optimized values for the exchange coefficients of KGTAl\Ca ) 1.6, KGTH\Ca ) 140, and Qmax ) 0.74 meq (g DCW)-1. Linear plots of measured data against calculated values indicated an accurate description of both Al (r ) 0.99; Figure 4A) and Ca adsorption (r ) 0.90; Figure 4B). VOL. 39, NO. 14, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5249
FIGURE 2. pH dependency of (A) Al and (B) Ca adsorption to isolated root cell wall. Different symbols represent the different treatments in experiments 2 and 3: control (-Al, triangles), 100 µM AlCl3 (diamonds), and 100 µM AlCl3 plus 100 µM citrate (circles) or 100 µM malate (squares). Lines represent first-order linear regression.
FIGURE 3. Al adsorption to isolated root cell wall material in relation to adsorbed Ca at pH 3.50 (squares) and pH 4.00 (diamonds).
the exchange coefficient from 140 to 50 and gave a better estimation of the Ca adsorption in relation to pH (Figure 7). When including formation constants for Al-citrate in the calculation and using the same parameters (KGT and Qmax) as for the calculation of Al adsorption without organic anion, the model could not describe the measured data. Al adsorption to the cell wall in the presence of citric acid was severely overestimated and subsequently Ca adsorption was underestimated (data not shown). However, when the same KGTH\Ca and Qmax values were used as for Ca adsorption (50 and 0.45, respectively), resulting in an estimated value for KGTAl\Ca of 1, Al and Ca adsorption could be described very well by the Gaines-Thomas exchange model (Al/cit in Figures 8 and 9, respectively). Though the model description of Al adsorption in the presence of malate approached the measured data, the Ca adsorption was overestimated at higher pH (Al/mal in Figures 8 and 9, respectively). Insufficient data points were available for a reasonable verification of the model for malate.
Discussion When all data points for Al adsorption at the different pHs were plotted against the ratio of solution activities of Al3+ and H+, the curves from Figure 1 fused into one curve (Figure 5A). Calculated Ca2+ activities for these points were reasonably constant at 0.83 ( 0.05 mM over the whole pH range. The exchange model, with the use of the abovementioned parameters, could again describe the data, though the model somewhat underestimated the Al adsorption at higher {Al3+}{H+}-1 ratio. The fit was better when a small adjustment was made by raising the Qmax to 0.80 while keeping the same KGT values (Figure 5B). With the Al and Ca adsorption data from Figure 2, the KGT values, and the three different values for Qmax (0.66, 0.74, and 0.80 meq (g DCW)-1), a plot of calculated Al adsorption against pH showed a slightly better fit with Qmax ) 0.66 meq (g DCW)-1 at pH < 3.75 and the best fit with the larger Qmax values at higher pH (Figure 6). A Qmax of 0.74 meq (g DCW)-1 was accepted as the best overall fit for Al adsorption. Calculated Ca adsorption, in the presence of Al and at Qmax ) 0.74, approached measured values, though its increase with pH was slightly too steep (Figure 7, +Al Qmax 0.74). Ca adsorption in the absence of Al, as described by the top line in Figure 2B was, however, not so well described when using Qmax ) 0.74 meq (g DCW)-1 and KGTH\Ca ) 140 (Figure 7, -Al Qmax 0.74). Ca adsorption was severely underestimated at low pH and overestimated at pH > 3.75. An optimized Qmax value for Ca binding was 0.45 meq (g DCW)-1, which reduced 5250
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 39, NO. 14, 2005
The in vitro data presented here show that Al replaces most but not all Ca at the cell wall binding sites, with the total Al adsorption depending on the solution pH. Zheng and coworkers described in a recent paper a similar pectin-related and malate-sensitive Al adsorption to wheat root cell wall (29). The Al/Ca molar exchange ratio of 1:0.9 in our data is markedly higher than would be expected on the basis of a charge-neutral exchange with a ratio of 1:1.5 Al/Ca, indicating the displacement of an additional cation (i.e., H+). Two options for Ca-Al exchange on the cell wall exist which satisfy the model demands of charge-neutrality. For the first option, Al3+ adsorption has to be accompanied by desorption from the cell wall of additional protons besides Ca2+, to create sufficient negative binding sites for the Al3+ and to keep total charge unaltered. The second option would be binding of Al in the form of AlOH2+, causing subsequent proton release by hydrolysis to form new AlOH2+ and restore equilibrium in the solution. Which of the two options applies here could not immediately be concluded from the data, since both include Al/Ca exchange and proton release. Both options have been explored in the Gaines-Thomas exchange model used here but the use of AlOH2+ activity in the exchange model proved to be insufficiently sensitive to the pH changes to describe the Al adsorption in any way and was therefore not taken into further consideration. Aluminum accumulation in the form of polynuclear Al species, like Al13 (AlO4Al12(OH)24(H2O)127+), was not expected to have been involved
TABLE 3. Estimated Input Parameters and Gaines-Thomas Coefficients for Exchange of Al3+, Ca2+, and H+ on Isolated Root Cell Wall Materiala Qmax
{H+}
{Ca2+}
0.66
10-3.53 10-3.52
10-3.08
a
{Al3+} 10-4.28
[Ca]cw
[Al]cw
[H]cw
KGTCa\H
KGTAl\H
KGTAl\Ca
0.402 0.231
10-1.98
10-1.70
100.28
0.429
0.258
Solution activities are in mol L-1, Qmax and cell wall adsorption are in meq (g DCW)-1.
FIGURE 4. Plots of measured against calculated values for (A) Al and (B) Ca adsorption to isolated root cell wall material. Dashed lines are 1:1 reference lines of calculated values.
FIGURE 5. Plots of measured and calculated values for Al adsorption against the {Al3+} to {H+} ratio. Maximum number of adsorption sites, Qmax, was set at (A) 0.74 or (B) 0.80 meq (g DCW)-1. at the low pH range used here. At higher Al concentration and pH, however, Al13 can be formed and interact with carboxylic binding sites of the cell wall (30, 31). With Al3+ as the adsorbing Al species, and taking proton competition into account, the model described the adsorption of Al very well (Figure 6). Lowering the Qmax to 0.45 allowed a fairly good description of the Ca adsorption (Figure 7). The initial value for Qmax of 0.66 meq (g DCW)-1 was based on acid-base titrations over a wide pH range. This means that not only the readily dissociating carboxylic groups of the cell wall pectin were taken into account but also phenolic -OH groups and -NH2 or -SH groups of cell wall proteins, with a pK > 7 (32, 33). Phenolics were responsible for as much as 26% of the maximum theoretical CEC in titrations of cell wall material of Sphagnum russowii, whereas 58% of the CEC was attributed to pectic compounds (28). Appreciable amounts of phenolic compounds were found in root cell walls of Gramineae, which makes this an interesting fraction with respect to cell wall adsorption, since pectin content is generally low in Gramineae (11, 33). Also interesting is the
possible role of root exudation of phenolics in plant Al tolerance (34). A variety of proteins is present in the cell wall, often cross-linked into the wall (35). It is impossible to estimate the extent of protein contribution to cell wall CEC without protein determination. Even if total protein content would be known, the effect would depend on the charge of the amino acids: the presence of glutamic and aspartic acid, with a pKa of 4.3 and 3.9, respectively, may have added to the cell wall CEC at the low pH range, whereas most other amino acids have a higher pKa (28, 36). The cell wall protein extensin is a potential candidate for binding Al to the cell wall, since it readily bound Al in in vitro studies (8). The importance of these sites for Al binding to cell wall material needs to be investigated and may vary with plant species. Isolated cell walls have responded with different affinities to a range of cations, leading to different estimates for total CEC (37-39). Sites with a high proton affinity may become visible in adsorption experiments with a high affinity cation, like Al3+ in the experiments described in this paper, while Ca2+ may not be able to compete with H+, at the given [Ca]sol. VOL. 39, NO. 14, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5251
FIGURE 6. Simulation of Al adsorption to isolated cell wall material in solutions containing 100 µM AlCl3 and 1 mM CaCl2, at pH 3.004.25. The maximum number of adsorption sites, Qmax, was set at 0.66, 0.74, or 0.80 meq (g DCW)-1; KGTH\Ca ) 140, KGTAl\Ca ) 1.6.
FIGURE 7. Simulations of Ca adsorption to isolated cell wall material in solutions containing 1 mM CaCl2 and 0 or 100 µM AlCl3, at pH 3.00-4.25. Model parameters (Qmax, KGTH\Ca, and KGTAl\Ca) for the different simulations were set at (0.74, 140, -) and (0.45, 50, -) for Ca and at (0.74, 140, 1.6) for Ca + Al. The lower Qmax, resulting from the data on Ca adsorption in the absence of Al, is likely to represent the cation exchange capacity of the pectic groups in the cell wall. If additional Al adsorption sites are very different from the pectic carboxylic groups, the KGT values derived here for Al exchange must be regarded as a combined exchange coefficient for all groups. This basically refutes the second assumption of the GainesThomas model, i.e., that the exchange model is homogeneous. Yet, by using the different Qmax values within the Gaines-Thomas model, a simplified heterogeneous model is created. More detailed analysis of Al adsorption to plant cell walls may lead to new exchange coefficients, one for each specific binding site, which can then be included in a truly heterogeneous adsorption model, like the NICA (nonideal competitive adsorption (40)) model. This model has been used by Plette (41) to describe competitive binding of Cd2+, Zn2+, Ca2+, and H+ to cell walls of gram-positive bacteria, which contained both carboxylic and amino-type binding sites. Assuming that Al displaced protons and not Ca from the non-carboxylic sites, the Al/Ca exchange ratio for the carboxylic sites decreases from 1:0.9 to a yet unknown value. Blamey and co-workers found an Al/Ca exchange ratio of 1.65 when using a Ca-pectate gel (42, 43). This exchange 5252
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 39, NO. 14, 2005
FIGURE 8. Simulations of Al adsorption to isolated cell wall material in solutions containing 1 mM CaCl2 and 100 µM AlCl3, plus 0 organic anion (Al), 100 µM citrate (Al/cit), or 100 µM malate (Al/mal), at pH 3.00-4.25. Model parameters Qmax, KGTH\Ca, and KGTAl\Ca for the different simulations were set at 0.74, 140, 1.6 for Al, 0.45, 50, 1 for Al/cit, and 0.74, 140, 1.6 for Al/mal, respectively.
FIGURE 9. Simulations of Ca adsorption to isolated cell wall material in solutions containing 1 mM CaCl2 (Ca), 1 mM CaCl2, and 100 µM AlCl3 plus 100 µM of citrate (Al/cit) or malate (Al/mal), at pH 3.004.25. Model parameters Qmax, KGTH\Ca, and KGTAl\Ca for the different simulations were set at 0.45, 50, - for Ca, 0.45, 50, 1 for Al/cit, and 0.74, 140, 1.6 for Al/mal, respectively. implies the need for an additional adsorbing cation, such as H+, for charge-neutrality. If Al-Ca exchange at the carboxylic sites occurred at this ratio in the experiments described here, it was masked by a net proton release from non-carboxylic sites. Additionally, pectins in solution can behave differently from cell wall pectin (11), which may cause a discrepancy between results for adsorption to cell walls and to pectate. The curves for Al and Ca (-Al) adsorption in Figures 8 and 9 appear at first sight to be almost identical, which would mean a similar pH dependency of adsorption of Al and Ca. This would be in sharp contrast to the higher affinity of pectins for trivalent cations, which in the case of Al3+ is expected to increase the rigidity of cell wall cross-linking and restrict elongation. It would also contradict the relative pH independence of Al accumulation found for Chara corallina cell walls (44). However, when comparing the curves one should bear in mind that any increase in Al3+ adsorption involved desorption of both Ca2+ and H+, whereas the Ca adsorption in the absence of Al depended solely on the pH. Al adsorption was therefore relatively less sensitive to the pH, though not pH independent. The pH dependency of Al adsorption to
the cell wall material implies that a high solution [Al3+], as found in very acid mineral soils, will not irrevocably lead to high Al accumulation in plant root cell walls. Although a decrease in pH can to some extent alleviate Al toxicity by preventing its accumulation in the plant root (34, 45, 46), the competition mechanism between Al3+ and H+ is not likely to reduce the negative effects of extreme soil acidity. Under very acid conditions H+ replaces Al3+ as a major cause of cell wall cation-displacement and growth inhibition (47, 48). In the presence of citric acid, Al3+ activity and Al adsorption was low and Ca adsorption could be described with the exchange parameters for Ca adsorption without Al, indicating that under these circumstances Al and Ca only occupied the pectic binding sites. The difference between the Ca adsorption -Al and that of +Al/citrate is fully covered by the lowlevel adsorption of Al on the cell wall. The effect of malate is less well defined with the model, although Al3+ activity according to speciation calculation should be almost as much reduced as with citrate. The discrepancy between Al 3+ activity and Al adsorption may be contributed to inadequacy of the available equilibrium constant for Al-malate, which was not determined at the standard 25 °C. More appropriately derived values may lead to a better fit of the model description for Al adsorption in the presence of malate. Production and exudation of organic anions, like citrate and malate, is considered to be an important plant mechanism to tolerate toxic aluminum. Preventing Al3+ from interacting with root compartments such as the cell wall, by forming complexes with the toxic metal, is a plausible explanation for aluminum detoxification. However, high proton concentrations not only decrease Al adsorption to the cell walls but will also lead to a diminished formation of Al-citrate complexes. This means that exudation of organic anions such as citrate may be effective in preventing Al cell wall adsorption at a pH around 4 but it will lose its significance with decreasing pH.
Acknowledgments We thank Dr. LiPing Weng for her assistance in the adsorption simulations and Drs. Nell Romanova and Luuk Koopal of the Laboratory of Physical Chemistry and Colloid Science in Wageningen for providing the cell wall titration data and for stimulating discussions.
(10)
(11)
(12) (13) (14)
(15)
(16) (17)
(18) (19) (20)
(21) (22)
(23) (24)
Literature Cited (1) Silva, I. R.; Smyth, T. J.; Raper, C. D.; Carter, T. E.; Rufty, T. W. Differential aluminum tolerance in soybean: an evaluation of the role of organic acids. Physiol. Plant. 2001, 112, 200-210. (2) Ryan, P. R.; Reid, R. J.; Smith, F. A. Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity. Plant Physiol. 1997, 113, 1351-1357. (3) Tabuchi, A.; Matsumoto, H. Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol. Plant. 2001, 112, 353-358. (4) Rengel, Z. Role of dynamics of intracellular calcium in aluminium-toxicity syndrome. New Phytol. 2003, 159, 295-314. (5) Horst, W. J. The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Z. Pflanzenerna¨hr. Bodenk. 1995, 158, 419-428. (6) Ma, J. F.; Yamamoto, R.; Nevins, D. J.; Matsumoto, H.; Brown, P. H. Al binding in the epidermis cell wall inhibits cell elongation of okra hypocotyl. Plant Cell Physiol. 1999, 40, 549-556. (7) Schmohl, N.; Horst, W. J. Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Environ. 2000, 23, 735-742. (8) Kenjebaeva, S.; Yamamoto Y.; Matsumoto, H. The impact of aluminium on the distribution of cell wall glycoproteins of pea root tip and their Al-binding capacity. Soil Sci. Plant Nutr. 2001, 47, 629-636. (9) Kinraide, T. B.; Ryan, P. R.; Kochian, L. V. Interactive effects of Al3+, H+, and other cations on root elongation considered in
(25) (26)
(27) (28) (29)
(30) (31) (32) (33)
(34)
terms of cell-surface electrical potential. Plant Physiol. 1992, 99, 1461-1468. Horst, W. J.; Schmohl, N.; Kollmeier, M.; Baluska, F.; Sivaguru, M. Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 1999, 215, 163-174. Carpita, N. C.; Gibeaut, D. M. Structural models of primary-cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 1993, 3, 1-30. Kutschera, U. The current status of the acid-growth hypothesis. New Phytol. 1994, 126, 549-569. Blamey, F. P. C. A role for pectin in the control of cell expansion. Soil Sci. Plant Nutr. 2003, 49, 775-783. Chang, Y. C.; Yamamoto, Y.; Matsumoto, H. Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant Cell Environ. 1999, 22, 1009-1017. Schofield, R. M. S.; Pallon, J.; Fiskesjo¨, G.; Karlsson, G.; Malmqvist, K. G. Aluminum and calcium distribution patterns in aluminumintoxicated roots of Allium cepa do not support the calciumdisplacement hypothesis and indicate signal-mediated inhibition of root growth. Planta 1998, 205, 175-180. Pellet, D. M.; Papernik, L. A.; Kochian, L. V. Multiple aluminumresistance mechanisms in wheat. Roles of root apical phosphate and malate exudation. Plant Physiol. 1996, 112, 591-597. Pin ˜ eros, M. A.; Magalhaes, J. V.; Carvalho Alves, V. M.; Kochian, L. V. The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol. 2002, 129, 1194-1206. Hue, N. V.; Craddock, G. R.; Adams, F. Effect of organic acids on aluminum toxicity in subsoils. Soil Sci. Soc. Am. J. 1986, 50, 28-34. Motekaitis, R. J.; Martell, A. E. Complexes of aluminum(III) with hydroxy carboxylic acids. Inorg. Chem. 1984, 23, 18-23. Wehr, J. B.; Menzies, N. W.; Blamey, F. P. C. Model studies on the role of citrate, malate and pectin esterification on the enzymatic degradation of Al- and Ca-pectate gels: possible implications for Al-tolerance. Plant Physiol. Biochem. 2003, 41, 1007-1010. Sentenac, H.; Grignon, C. A model for predicting ionic equilibrium concentrations in cell walls. Plant Physiol. 1981, 68, 415-419. Keizer, M. G.; De Wit, J. C. M.; Meeussen, J. C. L.; Bosma, W. J. P.; Nederlof, M. M.; Van Riemsdijk, W. H.; Van der Zee, S. E. A. T. M. ECOSAT; Technical Note of the Department of Soil Science and Plant Nutrition; Wageningen Agricultural University: Wageningen, The Netherlands, 1992. Blamey, F. P. C.; Ostatek-Boczynski, Z.; Kerven, G. L. Ligand effects on aluminium sorption by calcium pectate. Plant Soil 1997, 192, 269-275. Lindsay, W. L. Chemical Equilibria in Soils; John Wiley and Sons: New York, 1979. Martell, A. E.; Smith, R. M. Critical Stability Constants, 1st ed.; Plenum Press: New York, 1979; vol. 3, pp 124-126. Nordstrom, D. K.; May, H. M. Aqueous equilibrium data for mononuclear aluminum species. In The Environmental Chemistry of Aluminum; Sposito, G., Ed.; CRC Press: Boca Raton, FL, 1989; pp 29-53. Grignon, C.; Sentenac, H. pH and ionic conditions in the apoplast. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991, 42, 103-128. Richter, C.; Dainty, J. Ion behavior in plant cell walls. I. Characterization of the Sphagnum russowii cell wall ion exchanger. Can. J. Bot. 1989, 67, 451-459. Zheng, S. J.; Lin, X.; Yang, J.; Liu, Q.; Tang, C. The kinetics of aluminum adsorption and desorption by root cell walls of an aluminum resistant wheat (Triticum aestivum L.) cultivar. Plant Soil 2004, 261, 85-90. Kinraide, T. B. Identity of the rhizotoxic aluminium species. Plant Soil 1991, 134, 167-178. Xia, H.; Rayson, G. Investigation of aluminum binding to a Datura innoxia material using 27Al NMR. Environ. Sci. Technol. 1998, 32, 2688-2692. Meychik, N. R.; Yermakov, I. P. Ion exchange properties of plant root cell walls. Plant Soil 2001, 234, 181-193. Se´ne´, C. F. B.; McCann, M. C.; Wilson, R. H.; Grinter, R. Fourier transform Raman and Fourier transform infrared spectroscopy. An investigation of five higher plant cell walls and their components. Plant Physiol. 1994, 106, 1623-1631. Barcelo´, J.; Poschenrieder, C. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms
VOL. 39, NO. 14, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5253
(35) (36) (37)
(38) (39) (40)
(41)
(42)
of aluminium toxicity and resistance: a review. Environ. Exp. Bot. 2002, 48, 75-92. Cassab, G. I. Plant cell wall proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49, 281-309. Rubini, P.; Lakatos, A.; Champmartin, D.; Kiss, T. Speciation and structural aspects of interactions of Al(III) with small biomolecules. Coord. Chem. Rev. 2002, 228, 137-152. Gillet, C.; Voue´, M.; Cambier, P. Conformational transitions and modifications in ionic exchange properties induced by alkaline ions in the Nitella flexilis cell wall. Plant Cell Physiol. 1994, 35, 79-85. Gillet, C.; Voue´, M.; Cambier, P. Site-specific counterion binding and pectic chains conformational transitions in the Nitella cell wall. J. Exp. Bot. 1998, 49, 797-805. Richter, C.; Dainty, J. Ion behavior in plant cell walls. IV. Selective cation binding by Sphagnum russowii cell walls. Can. J. Bot. 1990, 68, 773-781. Benedetti, M. F.; Milne, C. J.; Kinniburgh, D. G.; van Riemsdijk, W. H.; Koopal, L. K. Metal ion binding to humic substances: application of the non-ideal competitive adsorption model. Environ. Sci. Technol. 1995, 29, 446-457. Plette, A. C. C.; Benedetti, M. F.; van Riemsdijk, W. H. Competitive binding of protons, calcium, cadmium and zinc to isolated cell walls of a gram-positive soil bacterium. Environ. Sci. Technol. 1996, 30, 1902-1910. Blamey, F. P. C.; Dowling, A. J. Antagonism between aluminium and calcium for sorption by calcium pectate. Plant Soil 1995, 171, 137-140.
5254
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 39, NO. 14, 2005
(43) Ostatek-Boczynski, Z.; Kerven, G. L.; Blamey, F. P. C. Aluminium reactions with polygalacturonate and related organic ligands. Plant Soil 1995, 171, 41-45. (44) Taylor, G. J.; McDonald-Stephens, J. L.; Hunter, D. B.; Bertsch, P. M.; Elmore, D.; Rengel, Z.; Reid, R. J. Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol. 2000, 123, 987-996. (45) Kinraide, T. B. Aluminum enhancement of plant growth in acid rooting media. A case of reciprocal alleviation of toxicity by two toxic cations. Physiol. Plant. 1993, 88, 619-625. (46) Kinraide, T. B. Toxicity factors in acidic forest soils: attempts to evaluate separately the toxic effects of excessive Al3+ and H+ and insufficient Ca2+ and Mg2+ upon root elongation. Eur. J. Soil Sci. 2003, 54, 323-333. (47) Kidd, P. S.; Proctor, J. Why plants grow poorly on very acid soils: are ecologists missing the obvious? J. Exp. Bot. 2001, 52, 791799. (48) Koyama, H.; Toda, T.; Hara, T. Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity. J. Exp. Bot. 2001, 52, 361-368.
Received for review November 26, 2004. Revised manuscript received April 29, 2005. Accepted May 5, 2005. ES048138V
