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Title: Plasma membrane surface potential: dual effects upon ion uptake and toxicity

item WANG, PENG - Chinese Academy Of Sciences
item Kinraide, Thomas
item ZHOU, DON-MEI - Chinese Academy Of Sciences
item KOPITTKE, PETER - Queensland University - Australia
item PEIJNENBURG, WJGM - Leiden University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/7/2010
Publication Date: 11/30/2010
Citation: Wang, P., Kinraide, T.B., Zhou, D., Kopittke, P.M., Peijnenburg, W. 2010. Plasma membrane surface potential: dual effects upon ion uptake and toxicity. Plant Physiology. 155:808-820.

Interpretive Summary: The acquisition of nutrients and the avoidance of toxicants by plants is an important problem in agricultural production and human health. The bioavailability of nutrients and toxicants is determined by plant characteristics and by the environment. For example, copper, both a nutrient and a toxicant, is accumulated in some plants more than in others, and in 'hard' waters (high concentration of calcium and magnesium) copper is much less available (and less intoxicating) than copper in 'soft' waters. Toxicologists have adopted the Biotic Ligand Model (BLM) to interpret and predict toxicant bioavailability. The model states that ameliorative ions (e.g., calcium) alleviate toxicity by competing with toxicants (e.g., copper) for a cell-surface binding site. The BLM is only a partial explanation and it ignores the great importance of cell electrical phenomena. The contribution of the present study is the extension of our understanding of plant and environmental determinants of nutrient and toxicant acquisition. In particular, the study demonstrates that cell-surface electrical potentials influence the uptake or avoidance of charged solutes in two distinct ways. This knowledge is essential for improved management practices and plant breeding and selection for production in nutrient-poor, phosphate retentive, acidic soils.

Technical Abstract: Electrical properties of plasma membranes (PMs), partially controlled by the ionic composition of the bathing medium, play significant roles in the distribution of ions at the exterior surface of PMs and in the transport of ions across PMs. The effects of coexistent cations (commonly Al3+, Ca2+, Mg2+, H+, and Na+) on the uptake and toxicity of these and other ions (such as Cu2+, Zn2+, Ni2+, Cd2+, and H2AsO4-) to plants were studied in terms of the electrical properties of PMs. Increased concentrations of cations or decreased pH in rooting media, whether in solution culture or soils, reduced the negativity of the electrical potential at the PM exterior surface (Psi). This reduction decreased the activities of metal cations at the PM surface and increased the activities of anions such as H2AsO4–. Further, the reduced Psi negativity increased the surface-to-surface transmembrane potential difference (Em,surf), thus increasing the electrical driving force for cation uptake and decreasing the driving force for anion uptake across PMs. Analysis of measured uptake and toxicity of ions using the developed electrostatic models provides evidence that uptake and toxicity are functions of the dual effects of Psi (i.e., altered PM-surface ion activity and Em,surf gradient). This study provides novel insights into the mechanisms of plant-ion interactions and extends current theory to evaluate ion bioavailability and toxicity, indicating its potential utility in risk assessment of metal(loid)s in natural waters and soils.