Surface Electrical Potentials of Root Cell Plasma Membranes: Implications for Ion Interactions, Rhizotoxicity, and Uptake

Abstract

Many crop plants are exposed to heavy metals and other metals that may intoxicate the crop plants themselves or consumers of the plants. The rhizotoxicity of heavy metals is influenced strongly by the root cell plasma membrane (PM) surface's electrical potential (ψ₀). The usually negative ψ₀ is created by negatively charged constituents of the PM. Cations in the rooting medium are attracted to the PM surface and anions are repelled. Addition of ameliorating cations (e.g., Ca2+ and Mg2+) to the rooting medium reduces the effectiveness of cationic toxicants (e.g., Cu2+ and Pb2+) and increases the effectiveness of anionic toxicants (e.g., SeO₄2- and H₂AsO₄-). Root growth responses to ions are better correlated with ion activities at PM surfaces ({IZ}₀) than with activities in the bulk-phase medium ({IZ}_b) (IZ denotes an ion with charge Z). Therefore, electrostatic effects play a role in heavy metal toxicity that may exceed the role of site-specific competition between toxicants and ameliorants. Furthermore, ψ₀ controls the transport of ions across the PM by influencing both {IZ}₀ and the electrical potential difference across the PM from the outer surface to the inner surface (E_m,surf). E_m,surf is a component of the driving force for ion fluxes across the PM and controls ion-channel voltage gating. Incorporation of {IZ}₀ and E_m,surf into quantitative models for root metal toxicity and uptake improves risk assessments of toxic metals in the environment. These risk assessments will improve further with future research on the application of electrostatic theory to heavy metal phytotoxicity in natural soils and aquatic environments.

Figure 1

Schematic diagram of electrical profiles and ion distributions at a plant root cell surface, as described in the text. Cations are denoted by M^z+ (in red circle), and anions are denoted by M^z− (in green circle). −R⁻ and −P⁰ denote negatively charged and uncharged membrane components exposed at the outer surface of the plasma membrane (PM). The solid curve represents the profile of electrical potential from the external medium to the inner surface of the PM; The dashed curve illustrates this profile after the addition of surface-depolarizing solutes to the external medium. E_m is the transmembrane electrical potential difference from the bulk solution to the cell interior; ψ₀ is the potential difference between the PM outer surface and the external medium; E_m,surf is the potential difference from the plasma membrane exterior surface to the membrane interior; and ψ_0,cyt is the potential difference between the PM inner surface and the cell cytoplasm. ψ₀ and E_m,surf are altered, but ψ_0,cyt and E_m remain constant.

Figure 2

Responses of root cell plasma membrane (PM) surface electrical potential (ψ₀) to increasing concentrations of Ca²⁺, K⁺, and H⁺ in the cell-bathing media, which contain a background of 0.23 mM Ca²⁺, 0.22 mM Mg²⁺, 0.97 mM Na⁺, 0.44 mM K⁺ and pH = 6.0. These ψ₀ values were calculated by the Gouy-Chapman-Stern (GCS) model. Data were obtained from Wang et al. [29].

Figure 3

Relative root elongation (RRE, %) for wheat seedlings in response to Zn²⁺ treatments under different pH values (4.5, 5.5, and 6.1) or Ca²⁺ concentrations (0.05, 0.1, and 0.5 mM). Metal ion activities were expressed as ion activities in bulk-phase solutions ({Zn²⁺}_b) or activities at the PM surface ({Zn²⁺}₀). The equation RRE = 100/exp[(a{Zn²⁺}_b)^b] (Equation (8)) was used in (A); RRE = 100/exp[(a{Zn²⁺}₀)^b] (Equation (9)) was used in (B); RRE = 100/exp[(a(1 + c ψ₀){Zn²⁺}₀)^b] (Equation (10)) was used in (C); and RRE = 100{1 − 1/exp(p{Ca²⁺}₀)}/exp[(a(1 + c ψ₀){Zn²⁺}₀)^b] (Equation (11)) was used in (D). The dashed line in (D) shows the 1:1 slope relationship. Data were obtained from Wang et al. [12,35].

Figure 4

Metal accumulation in wheat seedling roots in response to Cu²⁺ treatments under different values for pH (5.1, 5.5, and 6.0) and Ca concentration (0.25, 1.0, and 4.0 mM). Metal ion activities were expressed as ion activities in bulk-phase solutions ({Cu²⁺}_b) or activities at the PM surface ({Cu²⁺}₀). The Michaelis-Menten Equation Cu uptake = a{Cu²⁺}_b/(K_m + {Cu²⁺}_b) (Equation (12)) was used in (A); Cu uptake = a{Cu²⁺}₀/(K_m + {Cu²⁺}₀) (Equation (13)) was used in (B); and Cu uptake = a(1 + b ψ₀){Cu²⁺}₀/(K_m + {Cu²⁺}₀) (Equation (14)) was used in (C). Data were obtained from Wang et al. [13].

Figure 5

The calculated PM surface activities of H₂AsO₄⁻ ({H₂AsO₄⁻}₀) at 1.0 µM NaH₂AsO₄, and the calculated PM surface electrical potential (ψ₀) in response to different Ca²⁺ activities ({Ca²⁺}_b) in test solutions, which contain a background of 0.27 mM Ca²⁺, 0.26 mM Mg²⁺, 1.26 mM Na⁺, and 0.52 mM K⁺ at pH 6.0.

Figure 6

Relative root elongation (RRE, %) and root metal accumulation in wheat seedlings in response to NaH₂AsO₄ treatments under different pH and Mg levels. Ion activities were expressed as activities in the bulk-phase solutions ({As(V)}_b) and at the PM surface ({As(V)}₀). The Weibull Equation RRE = 100/exp[(a{As(V)}_b)^b] (Equation (15)) was used in (A); and the Equation RRE = 100/exp[(a{As(V)}₀)^b] (Equation (16)) was used in (B); The Michaelis-Menten equation as Uptake = a{As(V)}_b/(K_m + {As(V)}_b) (Equation (17)) was used in (C); and the equation as Uptake = a{As(V)}₀/(K_m + {As(V)}₀) (Equation (18)) was used in (D). Data were obtained from Wang et al. [13,29].

Figure 7

Comparison of the measured (A) and predicted (B) root length (RL) when wheat seedlings were exposed to Zn-Co mixtures. Predicted RL was based upon extended multiplicative models using ion activities at PM surfaces ({Zn²⁺}₀ and {Co²⁺}₀). The solid lines show the linear regression. The details of the coefficients c and e (Equation (19)) and the function f({H⁺}₀,{Zn²⁺}₀,{Co²⁺}₀) (Equation (20)) are described in Table S2. Data were obtained from Wang et al. [12].