Aluminum, a Friend or Foe of Higher Plants in Acid Soils

Abstract

Aluminum (Al) is the most abundant metal in the earth's crust, but its availability depends on soil pH. Despite this abundance, Al is not considered an essential element and so far no experimental evidence has been put forward for a biological role. In plants and other organisms, Al can have a beneficial or toxic effect, depending on factors such as, metal concentration, the chemical form of Al, growth conditions and plant species. Here we review recent advances in the study of Al in plants at physiological, biochemical and molecular levels, focusing mainly on the beneficial effect of Al in plants (stimulation of root growth, increased nutrient uptake, the increase in enzyme activity, and others). In addition, we discuss the possible mechanisms involved in improving the growth of plants cultivated in soils with acid pH, as well as mechanisms of tolerance to the toxic effect of Al.

Keywords: acid soils; aluminum; aluminum toxicity; beneficial effect of aluminum; mechanisms of tolerance; metal; plant growth stimulation.

FIGURE 1

Soil acidification is a phenomenon determined by natural and anthropogenic factors. The decomposition of the organic matter, the imbalance of the N, S, and C cycles, the excess in the cation uptake on anions and the N fixation by the legumes influence the concentration of protons [H⁺] in the soil solution. Anthropogenic factors such as the use of fertilizers (nitrogen, phosphorus, and potassium, NPK), the use of acidifiers and aerosols (H₂S, H₂SO₄, HF, and Cl₂), and the emission of gasses (CO₂, NO₂, and SO₂) into the atmosphere by use of fossil energy give rise to environmental pollution. Such molecules find their way into soil and water bodies in the form of acid rain, causing acidification of soils and the release of Al ions in a form easily absorbed by the plant root system, which is extremely toxic. Also, nutrient deficiency (P, Mg, and K) and toxicity by other metals (Mn and Fe) may occur.

FIGURE 2

Aluminum abundance and speciation in the earth’s crust. (A) Different forms of Al in the soil and water. Aluminum is mainly found in the mineral form (aluminosilicates and aluminum oxides). In addition, Al can be found as precipitates or conjugated organic and inorganic, and molecular ions depending on the soil pH. (B) Al-speciation in soil solution. Al concentration and the speciation of Al depend on the pH and the chemical environment of the soil solution. However, a very toxic polynuclear Al species (^∗Al₁₃) depends on the total concentration of Al. Molecular aluminum (mononuclear) exists as hydroxyaluminum: Al/Al(H₂O)₆³⁺, AlOH²⁺, Al(OH)₂⁺, Al(OH)₃ y Al(OH)₄^- Trivalent aluminum (Al) is the most abundant form and has the greatest impact on plant growth at pH < 5. At pH > 5–6, the dominant species are AlOH²⁺ and Al(OH)₂⁺, which are not as toxic to plants as Al. When the pH is neutral, Al(OH)₃ or gibbsite occurs; however, it is non-toxic and relatively insoluble. Aluminate, Al(OH)₄^-, is the dominant specie when the pH is alkaline (pH > 7). (Kinraide, 1991; Delhaize and Ryan, 1995; Brautigan et al., 2012; Hagvall et al., 2015; Kisnieriené and Lapeikaité, 2015).

FIGURE 3

Effect of aluminum on plants and mechanisms of tolerance to stress by aluminum. (1) Toxicity of Al in plants. (2) Beneficial effect of Al in some taxas, mainly species adapted to acid soils. (3) Mechanisms of exclusion, resistance or alleviation of Al uptake, and (4) Mechanisms of internal tolerance to stress by Al in plants.