The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review

Abstract

Background: Aluminium (Al) toxicity is the most important soil constraint for plant growth and development in acid soils. The mechanism of Al-induced inhibition of root elongation is still not well understood, and it is a matter of debate whether the primary lesions of Al toxicity are apoplastic or symplastic.

Scope: The present review focuses on the role of the apoplast in Al toxicity and resistance, summarizing evidence from our own experimental work and other evidence published since 1995.

Conclusions: The binding of Al in the cell wall particularly to the pectic matrix and to the apoplastic face of the plasma membrane in the most Al-sensitive root zone of the root apex thus impairing apoplastic and symplastic cell functions is a major factor leading to Al-induced inhibition of root elongation. Although symplastic lesions of Al toxicity cannot be excluded, the protection of the root apoplast appears to be a prerequisite for Al resistance in both Al-tolerant and Al-accumulating plant species. In many plant species the release of organic acid anions complexing Al, thus protecting the root apoplast from Al binding, is a most important Al resistance mechanism. However, there is increasing physiological, biochemical and, most recently also, molecular evidence showing that the modification of the binding properties of the root apoplast contributes to Al resistance. A further in-depth characterization of the Al-induced apoplastic reaction in the most Al-sensitive zone of the root apex is urgently required, particularly to understand the Al resistance of the most Al-resistant plant species.

Fig. 1.

Relationships between (A) pectin and Al content, and (B) Al content and relative callose induction (digitonin = 100) of root sections of maize (Zea mays) and faba bean (Vicia faba). Roots were incubated for 3 h in nutrient solution ± 50 µm Al or 10 µm digitonin at pH 4·3. ***Significant at P < 0·001. From Horst et al. (2007).

Fig. 2.

Relationship between root elongation rate and the Al contents of three apoplastic fractions in 5 mm root tips of common bean genotype Quimbaya (Al-resistant) grown in a simplified nutrient solution containing 0·5 mm CaCl₂, 0·5 mm KCl, 8 µm H₃BO₃ and 20 µm Al for up to 24 h, pH 4·5. ***Significant at P < 0·001. From Rangel et al. (2009a).

Fig. 3.

Effect of Al on the flow rate of dextran-10,000-TR and dextran-40,000-TR in root xylem exudates of maize cv. Lixis. Al and fluorescent tracers were applied to the 1 cm root apex for 2 h including the 1 h exudate collection period. Values are means of 8–10 independent replicates ±s.e. Means with * indicate significant differences at P < 0·05 (Tukey test). From Sivaguru et al. (2006).

Fig. 4.

(A) Effect of Al supply on relative root growth (–Al = 100 %) of transgenic potato lines that differ in expression of PME. Different letters indicate significant differences between lines at P < 0·05 (Tukey test). (B) Relationship between relative root growth (–Al = 100 %) of potato genotypes (wild type and PME transformants) and Al contents, and (C) relationship between Al contents and Al-induced callose contents in root apices. Treatment of intact plants in nutrient solution for 24 h at pH 4·3. From Horst et al. (2007).

Fig. 5.

Effect of polyethylene glycol (PEG) treatment on relative (no PEG = 100) Al, La and Sr accumulation of 10 mm root tips of Al-sensitive common bean genotype VAX-1. Plants were pre-treated with PEG (150 g L⁻¹) for 8 h in a simplified solution (pH 4·5) containing 5 mm CaCl₂, 1 mm KCl and 8 mm H₃BO₃. Then the plants were supplied with 25 mm AlCl₃, 5 mm LaCl₃ or 2·5 mm SrCl₂ in the absence or presence of PEG (150 g L⁻¹) in the same nutrient solution for 1 h. The hydrated ionic diameters are indicated under the ions. Bars represent means ± s.d. (n = 4). (Z. Yang et al., Leibniz University Hannover, Germany, unpubl. res.)

Fig. 6.

Relationship between the contents of Al and oxalate in the water free-space fluid (WFSF) of adventitious buckwheat root tips. The WFSF was extracted by centrifugation of excised 10 mm root tips at 4000 g for 15 min. Plants were pre-treated for 0·5, 4 and 24 h at 75 µm Al in simplified nutrient solution (pH 4·3) containing 500 µm CaCl₂, 8 µm H₃BO₃ and 100 µm K₂SO₄. Points represent single values. **Significant at P < 0·01. (B. Klug and W. J. Horst, Leibniz University Hannover, Germany, unpubl. res.)