The BnALMT1 and BnALMT2 Genes from Rape Encode Aluminum-Activated Malate Transporters That Enhance the Aluminum Resistance of Plant Cells

Abstract

The release of organic anions from roots can protect plants from aluminum (Al) toxicity and help them overcome phosphorus (P) deficiency. Our previous findings showed that Al treatment induced malate and citrate efflux from rape (Brassica napus) roots, and that P deficiency did not induce the efflux. Since this response is similar to the malate efflux from wheat (Triticum aestivum) that is controlled by the TaALMT1 gene, we investigated whether homologs of TaALMT1 are present in rape and whether they are involved in the release of organic anions. We isolated two TaALMT1 homologs from rape designated BnALMT1 and BnALMT2 (B. napus Al-activated malate transporter). The expression of these genes was induced in roots, but not shoots, by Al treatment but P deficiency had no effect. Several other cations (lanthanum, ytterbium, and erbium) also increased BnALMT1 and BnALMT2 expression in the roots. The function of the BnALMT1 and BnALMT2 proteins was investigated by heterologous expression in cultured tobacco (Nicotiana tabacum) cells and in Xenopus laevis oocytes. Both transfection systems showed an enhanced capacity for malate efflux but not citrate efflux, when exposed to Al. Smaller malate fluxes were also activated by ytterbium and erbium treatment. Transgenic tobacco cells grew significantly better than control cells following an 18 h treatment with Al, indicating that the expression of BnALMT1 and BnALMT2 increased the resistance of these plant cells to Al stress. This report demonstrates that homologs of the TaALMT1 gene from wheat perform similar functions in other species.Aluminum (Al) toxicity is the primary factor limiting crop production on acidic soils. When the soil pH falls below 5.0 the soluble Al in the soil solution exists predominantly as the toxic trivalent cation Al 31 that can inhibit root growth in many species at micromolar concentrations . Some species have developed mechanisms to overcome Al-related stresses by either excluding Al from the root cells (resistance mechanisms) or by increasing their tolerance to Al once these cations have been absorbed by the roots (tolerance mechanisms). Exclusion mechanisms might involve the exudation of Al-chelating ligands, the binding of Al within the cell wall or mucilage, plant-induced pH changes in the rhizosphere that reduce the local concentration of Al 31 relative to other hydrolysis products, the selective permeability of the plasma membrane, or perhaps the efflux of Al itself from the root cells. Tolerance mechanisms might include the chelation of Al in the cytosol, the sequestration of Al in the vacuole or other organelles, or modifications to metabolism that allow cellular function to continue normally in the presence of Al (Foy et al., 1978;Taylor, 1991;Delhaize and Ryan, 1995;Horst, 1995;Kochian, 1995;Ma et al., 2001;Matsumoto, 2002).The mechanism of Al resistance that has been observed most commonly in monocotyledonous and dicotyledonous species involves the release of organic anions such as malate, citrate, and oxalate from roots (Miyasaka et a...

The BnALMT1 Protein that is an Aluminum-Activated Malate Transporter is Localized in the Plasma Membrane

“…The transcript of BnALMT1 and BnALMT2 was accumulated in the root, not shoot by Al in a concentration dependant manner. 20 This is similar to AtALMT1 19 but contrasts with TaALMT1 which is constitutively expressed in wheat and unaffected by Al treatment. 16 Our result also showed that neither BnALMT1 nor BnALMT2 is induced by P-deficiency.…”

“…16 Our result also showed that neither BnALMT1 nor BnALMT2 is induced by P-deficiency. 20 Therefore, we conclude that P-deficiency does not induce both BnALMT transcript accumulation and malate efflux in rape. 12,20 Overexpression of the BnALMT proteins in tobacco cells and Xenopus oocytes conferred an Al-induced malate efflux.…”

“…20 Therefore, we conclude that P-deficiency does not induce both BnALMT transcript accumulation and malate efflux in rape. 12,20 Overexpression of the BnALMT proteins in tobacco cells and Xenopus oocytes conferred an Al-induced malate efflux. Citrate was not released from the transgenic cells, indicating that the BnALMT proteins are specific for malate transport.…”

Review Genetic and molecular mechanisms of aluminum tolerance in plants

“…The Al-activated mechanism of malate exudation is well described in wheat (Delhaize et al, 1993;Sasaki et al, 2004), Arabidopsis (Hoekenga et al, 2006), Brassica napus (Ligaba et al, 2006), and rye (Collins et al, 2008), whereas the mechanism of Al tolerance in maize, soybean, sorghum, and barley involves mainly citrate release (Pellet et al, 1995;Yang et al, 2000;Magalhaes et al, 2007;Furukawa et al, 2007;Maron et al, 2010).…”

Foreword: Understanding how plants cope with acid soils

“…It encodes a novel anion channel that controls the aluminium-activated efflux of malate from root apices. Homologous genes conferring similar functions have been isolated in Arabidopsis (Hoekenga et al 2006), rape (Brassica napus L.; Ligaba et al 2006) and rye (Secale cereale L.; Collins et al 2008). Interestingly, the genes controlling citrate efflux in response to aluminium stress are members of a different family named the multi-drug and toxic compound extrusion (MATE) family.…”