Aluminum exclusion and aluminum tolerance in woody plants

Abstract

The aluminum (Al) cation Al(3) (+) is highly rhizotoxic and is a major stress factor to plants on acid soils, which cover large areas of tropical and boreal regions. Many woody plant species are native to acid soils and are well adapted to high Al(3) (+) conditions. In tropical regions, both woody Al accumulator and non-Al accumulator plants occur, whereas in boreal regions woody plants are non-Al accumulators. The mechanisms of these adaptations can be divided into those that facilitate the exclusion of Al(3) (+) from root cells (exclusion mechanisms) and those that enable plants to tolerate Al(3) (+) once it has entered the root and shoot symplast (internal tolerance mechanisms). The biochemical and molecular basis of these mechanisms have been intensively studied in several crop plants and the model plant Arabidopsis. In this review, we examine the current understanding of Al(3) (+) exclusion and tolerance mechanisms from woody plants. In addition, we discuss the ecology of woody non-Al accumulator and Al accumulator plants, and present examples of Al(3) (+) adaptations in woody plant populations. This paper complements previous reviews focusing on crop plants and provides insights into evolutionary processes operating in plant communities that are widespread on acid soils.

Keywords: acid soils; adaptation; aluminum; organic acids; resistance; tolerance; toxicity.

FIGURE 1

World acid soils and world forests. (A) pH of topsoil (0–30 cm), (B) pH of subsoil (30–100 cm), and (C) forest cover. Soil pH is presented in two classes: pH ≤ 4.5 (strongly acid soils) and pH 4.6–5.5 (moderately acid soils). Data were retrieved from the Harmonized World Soil Data Base (FAO/IIASA/ISRIC/ISS-CAS/JRC, 2012). Forest cover is presented in four classes: ≤5, 6–25, 26–75, and 76–100%. Data were retrieved from the Food Insecurity, Poverty and Environment Global GIS Database (FGGD; FAO and IIASA, 2007).

FIGURE 2

Mechanisms of plant roots to deal with Al³⁺ (modified from Jones and Ryan, 2003; Inostroza-Blancheteau et al., 2012). OA, organic acids; P, pectin; PME, pectin methylesterase.

FIGURE 3

Expression levels of ALS3 in tissues of Populus tremula treated with Al³⁺ for 2 days. (A) Expression levels in root, stem and leaf tissue after treatment with 0 or 500 μM Al³⁺. (B) Expression levels in the root tissue after treatment with 0, 50, 100, 250, 500, or 1000 μM Al³⁺ or La³⁺. Transcript levels were quantified by absolute qRT-PCR. Different letters indicate significant differences between treatments and elements: ANOVA; P < 0.05 (redrawn from Grisel et al., 2010).