Reevaluating the free-ion activity model of trace metal availability to higher plants

Abstract

The plant uptake and toxicity of many metals show a marked dependence on the aqueous speciation of the metal, and these responses often correlate best with the activity of the free metal ion. Exceptions to this generalization have been observed, however, and we sought to critically reexamine the theoretical foundation of the free-ion activity model (FIAM) of metal bioavailability to higher plants. Binding by an apoplastic functional group is often envisioned as a requisite step in the absorption or toxicity of a metal, and can be modeled in a variety of ways. Typically, however, speciation of the bulk solution is calculated without regard to such surface binding, even though it could influence the pertinent mass balance expressions. A more thorough treatment considers simultaneous formation of both the metal-ligand complex in solution (ML) and the metal-cell surface complex (M-X). Here, empirical conformity to the FIAM can be expected, but only under pivotal assumptions about the relative sizes of the test solution and the root biomass, and about the relative binding strength of L and -X. Moreover, empirical conformity to the FIAM does not preclude cell-surface binding of the complexed metal followed by ligand exchange (ML + -X ⇆ M-X + L), so that correlations between biological response and free metal-ion activity imply nothing about the molecular species that actually interacts with the cell surface. Computer simulations of Cu (II) binding by a model apoplastic ligand are used to illustrate these and other key features of the FIAM. Departures from the FIAM seem most likely when (i) the quantity of the metal-complexing ligand is limited (as may be the case in soil solution or in the rhizosphere), and/or (ii) the solution ligand is very weak.