Aluminum Tolerance in Plants and the Complexing Role of Organic Acids

Aluminum is the third most abundant element on Earth, constituting 7% of the land surface. In alkaline, neutral or slightly acidic soils, aluminum exists in forms not harmful to plant growth. When soil pH is 4.5-5 or lower, however, toxic soluble forms of Al accumulate to levels that inhibit root growth and function. In most of the world’s tropical areas where soil is acidic, aluminum toxicity limits the productivity of crop plants. Fortunately, cultivars of number of crop plants such as wheat, buckwheat, canola, oats, radish, rye, triticale and taro have evolved tolerance to aluminum toxicity. In a review article published in the June issue of Trends in Plant Science 6(6): 273-278, 2001, Jian Feng Ma at Kagawa University (Kagawa,Japan) and Peter Ryan and Emmanuel Delhaize at CSIRO (Canberra, Australia) discuss the various mechanisms of aluminum tolerance in these cultivars and offer suggestions on the directions of future research in this area.

The authors provide examples of Al-tolerant plant cultivars that are known to secrete organic acids such as citrate, oxalate and malate from their roots in response to Al treatment. These organic acid anions form sufficiently strong complexes with Al3+ to protect plant roots. The increased secretion of organic acids is confined to the root apical cells, resulting in a zone of detoxification that shields the root to ensure growth through acid soil.

Two patterns of organic acid secretion exist in Al-tolerant cultivars. In Pattern I, the organic acids exudates in the root apex are detectable within 15-30 minutes after exposure to Al. In Pattern II, there may be a delay of 4-10 hours between the exposure of a root apex to Al and the commencement of organic acid secretion. One cultivar of maize exhibits both patterns, producing first a rapid citrate secretion and then a delayed secretion continuing to increase over a period of 48 hours. The Pattern I mechanism is thought to involve pre-existing machinery for perception of Al and efflux of organic acids. By contrast, the Pattern II mechanism is thought to involve de novo gene activation and protein translation. Al-responsive genes might encode proteins involved in organic acid metabolism or efflux.

Changes in organic acid metabolism may occur in response to Al, and the authors describe several examples. In one case, rye roots demonstrated a 30% increase in citrate synthase activity following exposure to Al, although there was no increase in activities of phosphoenolpyruvate carboxylase, malate dehydrogenase or NADPH-dependent isocitrate dehydrogenase. In the Al-tolerant species Paraserianthes falcataria, mitochondrial citrate synthase gene expression and activity increased in response to Al. Some approaches to increase Al tolerance have thus involved manipulation of organic acid metabolic enzymes. For example, overexpression of carrot mitochondrial citrate synthase in Arabidopsis caused increased citrate synthase activity, increased production of citrate, and a 60% increase in citrate efflux.

Some species naturally accumulate high levels of Al in aboveground tissues. The authors cite one example of an extremely tolerant species found in tropical rainforests, Melastoma malabathricum. The presence of Al in soil actually stimulates growth of this plant. Since the binding affinity of Al3+ for ATP is almost 10.7 times stronger than that of Mg2+, this species must have mechanisms for the detoxification of intracellular Al3+. Other Al-accumulating species include buckwheat and hydrangea. The color of hydrangea sepals ranges from pink to blue depending upon the level of aluminum present in the soil; the blue color results from a complex of Al, delphinidin 3-glucoside and 3-caffeoylquinic acid.

The authors describe recent evidence showing that at least two of these three Al-accumulating species detoxify internal Al3+ by forming Al-organic acid complexes. Stable complexes between Al and organic acids are thought to reduce the level of Al in the cytosol and thus reduce cytotoxic effects. In buckwheat, ligand exchanges have been observed as various forms of Al-organic acids are transported throughout the plant. The intake of Al3+ by the roots is followed by the formation of a 1:3 Al-oxalate complex in the root cells. Al is transported through the xylem as Al-citrate. Another ligand exchange reaction occurs when Al-citrate is converted back to Al-oxalate in leaf cells before storage of the oxalate complex in the vacuole.

As Al toxicity remains a significant problem in agriculture, the authors advocate both proper land use strategies to avoid Al soil contamination and development of new cultivars for use on marginal soil. The authors suggest the utilization of other organic acid metabolic genes in addition to citrate synthase, which has already been a target of manipulation. To enhance organic acid efflux, the authors suggest that it may be necessary to overexpress an as-yet-unidentified gene encoding an organic acid transporter.

In conclusion, the authors note that many crop plants have no Al-tolerant cultivars. Creation of transgenic lines utilizing genes from Al-tolerant species may allow cultivation of such crops in Al-contaminated soil.

 

 

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