16.5.2  Aluminium and manganese toxicities

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Soil pH has a marked effect on nutrient availability (Figure 16.2) by affecting both solubility of soil minerals present and the ability of plant roots to absorb nutrients. Generally, a decrease in soil pH increases availability of cations, especially essential micronutrients, Fe, Mn, Cu and Zn. In contrast, availability of Mo decreases, often to such an extent that acid soils are deficient in plant-available Mo. Availability of P also decreases at low pH via fixation with hydrous oxides of Fe and Al, although reactions with Ca can also reduce P availablility around pH 8.5 (Figure 16.2).

(a)  Aluminium toxicity

Al toxicity has been recognised for over 60 years. Shortly after the turn of the twentieth century, soil scientists found Al present in solution leached from soils. However, later attention was given to hydrogen clays, and following development of glass electrodes research emphasis was placed on soil pH for many years — an example of technology driving science! Despite publication of research results between the late 1920s and late 1960s, deleterious effects of Al on plant growth did not attract interest again until the early 1970s. Some of those findings are outlined here.


Table 16.9

Al is the most common metal in the earth’s crust (8% of dry mass) and comprises some 7% of soils, where it has a complex chemistry. Al is an important component of aluminosilicate compounds, including clay particles. As soils acidify, Al dissolves from these solid forms, and enters solution with the potential to then become toxic (Table 16.9). Not all Al in the soil solution is toxic, however, providing challenges to biologists to identify those forms that are. Those shown to be toxic to plants include the inorganic Al monomers (Al3+, AlOH2+, Al(OH)2+) and the inorganic polycation AlO4Al12 (OH)24 (H2O)247+ (known as Al13).

The concentration of Al in the soil solution is often low (<50 µM), and activities of monomeric Al in the soil solution that reduce root growth have been found to range from 4 to 15 µM. A further challenge to analytical chemists is to develop techniques able to discriminate between toxic and non-toxic forms of Al, made all the more difficult because of the low concentration of toxic Al. This concentration has been calculated to be about 0.1 g Al in 1 m3 of soil (c. 12 µM Al or one-third of one part per million in the soil solution). The same 1 m3 of acid soil would contain a total of 70 kg Al.

Solubility of Al decreases dramatically with an increase in soil pH (Figure 16.16a), and the concentration of inorganic monomeric Al in solution is also affected by organic and inorganic anions. Complexes of Al with organic ligands of low relative molecular mass, especially citric and malic acids, are also considerably less toxic. Tolerant plants benefit from such chelating mechanisms. In addition, organic matter increases the concentration of fulvic and humic acids, resulting in the formation of Al fulvate and Al humate. These complexes are considerably less toxic than the inorganic monomeric species.


Figure 16.16 (a) Total concentration of all ionic species of Al in solution as a function of pH. In (b) a solution that initially contains 1000 μM CaCl2 and 100 μM AlCl3 (used to approximate a soil solution) shows a marked decrease in concentration of Al3+ from pH 4.0 to pH 6.0, and a change in relative activities of different inorganic monomeric Al species. Underlying equilibria responsible for such pH effects are summarised below. Values for pK coincide with the pH of a solution where the reaction mixture would be 50% dissociated. Increasing H+ ion concentration due to decreasing pH forces such equilibria towards Al3+, thus inducing Al toxicity.

Al3+ + H2O ⇔ AlOH2+ +H+         pK = 5.00
Al3+ + 2H2O ⇔ AlOH2+ +2H+     pK = 10.10

(Based on Kinraide 1990)

Biological effects of ions are often better related to activ-ity in solution rather than to concentration. In addition to soil pH effects on Al solubility, speciation of Al in solution changes with pH (Figure 16.16b). At pH 4.0, most of the inorganic monomeric Al is present as Al3+; this decreases with an increase in pH while the activities of the hydroxy Al species (AlOH2+, Al(OH)2+) increase. At alkaline pH, aluminate ions (e.g. Al(OH)4, Al(OH)52–) enter into solution but are not toxic to plant roots (Kinraide 1990).

Soluble Al in solution has a rapid effect on root growth, with the effects often visible within 2 d. Microscopically, decreased root growth may be evident within a few hours of exposure to Al, and changes in Golgi apparatus activity have been documented to occur within 5 h of placing roots in a solution containing Al. To be toxic, the root tip must be exposed to Al (Ryan et al. 1993).


Figure 16.17 Soybean root growth decreases markedly as the sum of activities of monomeric Al species in solution increases. (Based on Alva et al. 1986)

While the toxic effect of Al has been known for more than 60 years, the biochemical basis of Al toxicity has not been clarified. However, Al is known to exert its primary toxic effect on roots, initial effects including a reduction in root length (Figure 16.17) (through reduced cell elongation) and damage to cortical cells of the root epidermis near the root tip. Proliferation of root hairs, important for uptake of water, essential nutrients and for infection by N-fixing rhizobia in legumes, is severely reduced by Al at concentrations lower than those that reduce root growth. Proposals for the primary toxic effect have included reactions of Al with components of the cell wall, plasma membranes, cytoplasm and nucleus (Kochian 1995).

Visible effects of soluble Al on plant tops are considered to be a secondary effect through reduced nutrient uptake. Symptoms include those similar to deficiencies of Ca, Mg, Fe, and P, probably as a result of decreased root proliferation and of reduced root activity. Further secondary effects include a reduction in uptake of water, increased sensitivity to drought and decreased N2 fixation by nodulated legumes.

Plant species differ markedly in tolerance to soluble Al in the soil solution. As with toxicity, the biochemical basis of genetic tolerance of Al toxicity is not clearly understood. However, malic acid excretion by root apices of Al-tolerant wheat is known to be five- to ten-fold greater than that excreted by Al-sensitive wheat. Malic acid presumably complexes soluble Al, making it less toxic (Delhaize et al. 1993), and that capacity for excretion co-segregates with Al tolerance in progeny from crosses between near-isogenic lines. By implication, a single major gene is probably responsible for an Al tolerance that is functionally linked to Al stimulation of malic acid excretion (Delhaize et al. 1993).

(b)  Manganese toxicity

Mn, an essential element for plants (Section 16.3), is about the tenth most abundant element in the earth’s crust. Like Al, Mn chemistry in acid soils is complex, affected by both soil pH and soil redox potential. Mn occurs in rocks mostly in co-ordination with O2+ and as the divalent Mn2+ in soil solution and in natural waters. Biotic and abiotic oxidation occurs readily so that Mn does not generally occur to excess except in acid soils or in waterlogged soils (assuming there are sufficient Mn-containing minerals). Mn toxicity may occur following soil sterilisation due to loss of microorganisms that normally oxidise Mn2+.

Al is a root toxin, whereas high Mn is mainly toxic to shoots (at very high Mn concentration, root growth may be affected directly). Thus, unlike Al, which often has an immediate effect on root proliferation, Mn must accumulate in shoots to become toxic. Three types of symptoms result from Mn accumulation: dark-brown, necrotic spots on lower leaves, distortion of expanding leaves (possibly an induced Ca deficiency) and chlorosis of young leaves. Such chlorosis is often interpreted as an Fe deficiency due to reduced Fe uptake by roots due to excess Mn (Figure 16.8).

Considerable genetic differences in tolerance to high concentrations of plant-available Mn exist among plant species, and even among lines within a species. Such variation may occur via differences in root exclusion of excess Mn, complexation of Mn within roots, or shoot tolerance of high Mn. Sunflower, watermelon and cucumber all show shoot tolerance and even excrete Mn in a biologically inactive form around trichomes (hairs) on leaves and stems (Blamey et al. 1986).


Table 16.10

External Mn concentrations at which plant growth is reduced also vary greatly among plant species. In carefully controlled solution culture (Edwards and Asher 1982), the critical external concentration (i.e. the concentration required for 10% reduction in plant dry mass) in the two most sensitive species, maize and wheat, was 1.4 µM Mn (Table 16.10). In contrast, sunflower growth was only reduced with 65 µM Mn in solution. Likewise, the critical internal Mn concentrations varied also, from 200 mg kg–1 in maize to 5300 mg kg–1 in sunflower. Although cowpea and bean had a similar external critical concentration, cowpea was able to tolerate a much higher tissue Mn. A higher retention of Mn in roots of soybean enabled this species to tolerate a higher external Mn concentration than cotton.

(c)  Countering adverse effects of acid soils

Acid soil problems have been traditionally corrected via application of agricultural lime (CaCO3) or dolomite (CaCO3 + MgCO3). Such amelioration raises soil pH, reducing Al and Mn concentrations in the soil solution, as well as adding the essential nutrients Ca and Mg. Lime or dolomite is generally required to raise soil pH to a level at which Al or Mn toxic-ities no longer affect plant growth (often above pH 5.5). Rates required vary considerably depending on soil type, with clay soils requiring higher rates to increase soil pH (greater buffering capacity referred to earlier in connection with acidification). Moreover, lime requirements for sustainable agriculture vary with farming systems. For example, lime required (kg CaCO3 ha–1 year–1) to balance net acid accumulation is about: 0.8 for wool, 6.0 for lamb and 7–20 for
cereal enterprises (Slattery et al. 1991). Even though cereal production is not greatly acidifying, Australia’s average wheat crop of 15 million t would have removed alkalinity equivalent to 135000 t CaCO3 as well as 6000 t Ca, 18 000 t Mg and 66 000 t K (along with 330 000 t N, 42 000 t P and 26 000 t S) from the land. Most of the crop was used for human consumption either in Australian cities or overseas. There would be little return of these nutrients to their original fields.

Application of lime in Australia falls far below that required to balance losses of alkalinity. Annually, c. 0.5 million t of lime is used in Australia, but more like 2.25 million t are needed annually as prophylactic dressings (Land and Water Resources Research and Development Corporation 1995). Overliming is a potential problem, especially on sandy soils, due to reduced availability of essential micronutrients, especially Zn, while root diseases such as ‘Take all’ of cereals are exacerbated.

Amelioration of some acid soils is possible via application of gypsum (CaSO4.2H2O) which provides a readily soluble form of Ca. Leaching soluble Ca applied as gypsum may improve root growth in acid subsoil horizons. Application of Mo is also beneficial where this essential micronutrient is in short supply due to low pH.

Finally, breeding and selection for crop tolerance to acid soil limitations has immediate application in agriculture, but an understanding of factors involved is crucial because tolerance to one factor limiting growth on acid soils (Al toxicity) does not imply tolerance to another such as Mn excess or Mo deficiency.

(d)  Concluding remarks

Acid soil infertility is a major limitation to plant growth worldwide, especially in the humid tropics, subtropics and temperate zones. Infertility results primarily from toxicities of Al or Mn and from deficiencies of Ca, Mg, K, P and Mo. While there are many soils that are naturally acid, farming practices and industrial processes contribute to increased soil acidification. These include use of N fertilisers, especially where they exacerbate the loss of basic cations through leaching and crop removal, and growth of legumes, which increase soil N status. Acid rain is important in industrialised regions.

Two complementary approaches may be used to overcome the adverse effects of soil acidity. The first is amelioration of acid soils through application of lime or gypsum to arrest degradation occasioned by a loss of basic cations. Unless these basic cations are replaced, land degradation through acidification and nutrient decline is inevitable. The second is a quest for genotypes better adapted to acid soil conditions. Genetic ap-proaches alone simply buy time and will result in further soil acidification, but do offer a beneficial trade-off: tolerant plants would draw water and nutrients from acid subsoils which are difficult, if not impossible, to ameliorate any other way.