The relationship between magnesium status and aluminium toxicity in Arabidopsis

Abstract

Aluminium (Al3+) toxicity affects plant productivity on over 40% of the world’s arable land although the primary mechanism of Al3+ toxicity remains unclear. Previous studies have shown that ectopic expression of magnesium (Mg2+) transport genes in yeast and plants increases tolerance to Al3+, suggesting that Al3+ may directly inhibit Mg2+ uptake. The purpose of this study was to examine, using physiological, transgenic and genomic approaches, interactions between Mg2+ and Al3+ in Arabidopsis thaliana to determine how Mg2+ might be associated with the primary molecular mechanism of Al3+ toxicity in plants. The effects of Mg2+ starvation on plant growth, Mg2+ content, shoot chlorosis, root length and root morphology were distinct from those observed with Al3+ toxicity, suggesting that these two phenomena are not the same. In contrast, low pH and low pH+Al3+ (Al3+) toxicity were morphologically alike and additive. Mg2+-starved plants were highly sensitive to low pH/Al3+, while availability of media Mg2+ had few detectable mitigating effects. Therefore it appears that internal plant Mg2+ status is more important than short-term uptake of media Mg2+ in protecting against Al3+ stress. Transgenic Arabidopsis lines expressing Mg2+ transport genes from Escherichia coli (CorA) and Saccharomyces cerevisiae (ALR1) were generated. CorA plants had increased Mg2+ uptake, but reduced plant survival and growth phenotypes suggestive of disruptions to plant Mg2+ homeostasis. CorA plants were highly sensitive to low pH/Al3+ and Mg2+-starved CorA root tips resembled those treated with low pH/Al3+. Expression of a plant-optimized variant of ALR1, crALR1, resulted in plants with only mild phenotypes suggestive of altered Mg2+ transport; however these plants exhibited increased tolerance to low pH/Al3+. Together, these data show that altering Mg2+ uptake and distribution in plants specifically affects Al3+ sensitivity and implicates a process involving Mg2+ in the primary mechanism of Al3+ toxicity. Microarray analyses revealed similarities in biotic stress responses between Al3+ toxicity and Mg2+ starvation. Mg2+ and Al3+ differentially regulated genes associated with Ca2+ transport, pH homeostasis, auxin regulation and flavonoid biosynthesis. Three possible mechanisms of Al3+ toxicity are proposed: increased low pH toxicity, activation of plant glutamate receptors (GLRs) and disruptions to intracellular Mg2+. For each mechanism, Mg2+-regulated processes may be affected; initiating Ca2+-associated signal transduction cascades which alter plant development, particularly in the root tip.