The role of the plasma membrane in the response of plant roots to aluminum toxicity

Abstract

Al(3+), the predominant form of solubilized aluminum at pH values below 5.0, has been shown to exert a profound inhibitory effect on root elongation. Al is known to accumulate at the root apex. The plasma membrane represents the first potential target for Al toxicity, due to its pronounced binding to phospholipids. Al appears to alter both the structure and functions of the plasma membrane, and a great deal of research has been conducted concerning the interactions between Al and the plasma membrane. In this review, recent findings regarding the interactions between Al and the plasma membrane are described, specifically findings involving Al-induced alterations in the structure and function of the plasma membrane.

Keywords: acid soil; aluminum; plasma membrane; tolerance; toxicity.

Figure 1

Transient responses of ion fluxes to Al, measured in the elongation zone. (A) K⁺ fluxes, (B) H⁺ fluxes, (C) Cl⁻ fluxes. Data show the responses collected on ET8 plants (open symbols) and ES8 plants (closed symbols) after the addition of 50 µM Al, as shown. Positive values are defined as influxes, and negative values as effluxes. Error bars are s.e.m. (n = 6–8). (From ref. 23).

Figure 2

Effects of Al (50 µM) treatment duration in vivo (0, 3 and 6 h) on the H⁺-ATPase activity (A) and zeta potential (B) of PM vesicles isolated from specific 5 mm root segment fractions of squash. The plants were grown in Hoagland solution (1/5) adjusted to pH 4.5 for 5 days after germination. Al treatments were conducted in identical solutions, without P, and the plants were cultured in -P solution for at least 12 h prior to treatments. The 5 mm DFTT segments were constructed of approximately 600 individual plants and the isolated PM vesicles were pooled to increase the precision of the measurements. Values are expressed as means ± SE of three replicates, and are representative of two independent experiments. (From ref. 34).

Figure 3

Visualization of Al-induced alterations of PM properties and Al binding capacity of PM vesicles isolated from squash root apex (0–5 mm) using the Morin assay. (A) Calibration (standard) showing a range of Al concentration and the Al-induced fluorescence of control PM vesicles (top panel); after 50 µM Al treatment in vivo (middle panel); further addition of 50 µM in vitro (10 min) to the same PM vesicles (bottom panel). (B) Quantitative evaluation of the Morin fluorescence based on pixel intensity corresponding to the images presented in (A). Results of standard (top) and after in vivo and in vitro treatments (bottom). (From ref. 34).

Figure 4

Effects of various in vitro Al concentrations, 0, 2.5, 5 and 10 µM (A), and 20 and 50 µM (B) on the zeta potential of PM vesicles isolated from the root tip (apical 10 mm) of ET8 and ES8 grown without Al for 5 days. Five µg of the PM protein (pH 7.4) was treated with Al for 10 min in vitro, and the zeta potential was measured immediately afterwards. The electrophoresis medium was free of Al. The experiment was conducted three times independently, giving similar results. Values are means ± SE (n = 3). Asterisks show statistically different means (*p < 0.05; Student's t-test). (From ref. 35).

Figure 5

Effects of various Al concentrations (0, 2.5, 5 and 10 µM) in vitro on the relative H⁺-ATPase activity in PM vesicles isolated from the roots of ET8 (A) and ES8 (B). Seedlings were grown in Al-free 0.2 mM CaCl₂ solution, adjusted to a pH of 4.5 for 5 days after germination. The PM vesicles were isolated from the root tips (0–10 mm) and the region distal to the tip (10–20 mm). Five µg of the PM protein (pH 7.4) was then treated with various concentrations of Al for 10 min in vitro, and centrifuged for 1 hour at 100,000 g in order to minimize the carryover of Al from the treatment solution. This experiment was conducted three times, and values from representative experiments are expressed as means ± SE (n = 3). Asterisks indicate statistically different means (*p < 0.05, Student's t-test). (From ref. 35).

Figure 6

A schematic diagram illustrating a possible mechanism linking the Al-induced exudation of malate and changes in the properties of PM in Al-tolerant (ET8) and Al-sensitive (ES8) wheat lines. Exudation of malate via malate-permeable channels is accompanied by the hyperpolarization of zeta potential and the enhancement of H⁺-ATPase activity in Al-tolerant plants. In contrast, in Al-sensitive plants, more negative zeta potential than in Al-tolerant plants attracts more Al³⁺, causing the depolarization of zeta potential and the decrease in the pumping out of H⁺ through the PM. The activation of a malate-permeable channel and the H⁺-ATPase are indicated by arrows of increased thickness in the Al-tolerant plants.