Interactive Effects of Al³⁺, H⁺, and Other Cations on Root Elongation Considered in Terms of Cell-Surface Electrical Potential

Abstract

The rhizotoxicities of Al3" and of La3" to wheat (Triticum aestivum L.) were similarly ameliorated by cations in the following order of effectiveness: H -C3 > C2 > C1'. Among tested cations of a given charge, ameliorative effectiveness was similar except that Ca2' was slightly more effective than other divalent cations and H' was much more effective than other monovalent cations. H' rhizotoxicity was also ameliorated by cations in the order C3' > C2 > C1". These results suggest a role for cell-surface electrical potential in the rhizotoxicity of Al3", La3, H', and other toxic cations: negatively charged cell surfaces of the root accumulate the toxic cations, and amelioration is effected by treatments that reduce the negativity of the cell-surface electrical potential by charge screening or cation binding. Membrane whose toxicity has not been established. It may be impossible to differentiate formally the two hypotheses for H+ amelioration of Al toxicity or to establish the rhizotoxicity of all of the Al species (12), but in this article we shall argue that Al" is toxic and that Al3" toxicity, specifically, is ameliorated by H+ and other cations. The argument will rest upon new data that support the hypothesis that the negatively charged cell surfaces in the root accumulate A13+ and other toxic cations, and that amelioration is effected by treatments that reduce the negativity of the cellsurface electrical potential.Negative charges, located in the cell wall and on the plasma membrane, are carried on the carboxylate groups of cell-wall pectins, the residues of acidic amino acids in membrane proteins, and the phosphate groups of membrane phospholipids (16,19,23). The charges on the cell surface create electrical potential gradients that interact with the distribution of ions (5,18,19). Salts in the bathing medium reduce the negative surface potential in two ways: by cation binding and by charge screening. Because of the binding of H+ with carboxylate, phosphate, and amino groups, charge reversal of the plasma membrane surface can occur as the pH there drops below 4 (22). Divalent and polyvalent cations can also bind, and the latter can cause charge reversals at the membrane surface (1, 21). Charge screening occurs because coulombic attractions concentrate cations around the cell-surface negative charges. The effectiveness of the cations in charge screening increases with cation valence according to basic electrostatic models (5,18,19).Amelioration of Al toxicity by H+ and other cations can be interpreted as evidence of the influence of cell surface charge on Al toxicity, but another line of evidence also suggests the same conclusion. Several reports indicate that within closely related taxa, higher varietal sensitivity to Al corresponds to higher varietal cation exchange capacity of whole roots (8, 27, and

Plasma Membrane Surface Potential: Dual Effects upon Ion Uptake and Toxicity

“…Addition of Ca 2+ or Mg 2+ alleviated Al 3+ toxicity. Kinraide et al (1992) The addition of Ca 2+ or Mg 2+ or the reduction of pH will increase the surface activity of H 2 AsO 4 -and thus the uptake and toxicity of arsenic. H 2 AsO 4 -(arsenate) may become transformed in the roots into the even more toxic H 2 AsO 3 -(arsenite; Pickering et al, 2000).…”

“…Measured RRE of wheat seedlings exposed to Al 3+ affected by Ca 2+ and Mg 2+ . Data were taken from Kinraide et al (1992;experiment 14 petition), such mechanisms appear to be unimportant in many cases (Kinraide, 2006;Wang et al, 2008). In those cases, including those in this study, the dual effects of c 0 o are sufficient to explain the ion-toxicant interactions (Kinraide, 2006;Wang et al, 2008; this study).…”

Direct Evaluation of the Ca2+-Displacement Hypothesis for Al Toxicity

“…3). Kinraide et al (1992Kinraide et al ( , 1994 the electrostatic accumulation of a11 cations (including AI) toward the cell surface. A second prediction from those studies was that the inhibition of root growth should correlate more closely with the activity of A13+ at the membrane surface than with the activity of A1 in the bathing solution.…”

Sorption of Aluminum to Plasma Membrane Vesicles Isolated from Roots of Scout 66 and Atlas 66 Cultivars of Wheat

“…The stimulation of organic acid secretion by A13+ is quite specific. La3+ is highly rhizotoxic but fails to stimulate malate secretion in wheat (Delhaize et al, 1993), and A13+-tolerant and AI3+-sensitive genotypes are nearly equally sensitive to La3+ (Parker, 1988;Kinraide et al, 1992;Delhaize et al, 1993).…”

“…Treatments that reduce cell-surface negativity reduce the sensitivity of roots to cationic toxicants (Kinraide et al, 1992;Kinraide, 1994) and increase the sensitivity to at least one anionic toxicant, Se0,'- (Kinraide, 1994). Consequently, it was proposed decades ago that negative surface-charge densities may be lower in AI3+-tolerant genotypes (Vose and Randall, 1962).…”