Not all ALMT1‐type transporters mediate aluminum‐activated organic acid responses: the case of ZmALMT1 – an anion‐selective transporter

Abstract

SummaryThe phytotoxic effects of aluminum (Al) on root systems of crop plants constitute a major agricultural problem in many areas of the world. Root exudation of Al-chelating molecules such as low-molecular-weight organic acids has been shown to be an important mechanism of plant Al tolerance/resistance. Differences observed in the physiology and electrophysiology of root function for two maize genotypes with contrasting Al tolerance revealed an association between rates of Al-activated root organic acid release and Al tolerance. Using these genotypes, we cloned ZmALMT1, a maize gene homologous to the wheat ALMT1 and Arabidopsis AtALMT1 genes that have recently been described as encoding functional, Al-activated transporters that play a role in tolerance by mediating Al-activated organic acid exudation in roots. The ZmALMT1 cDNA encodes a 451 amino acid protein containing six transmembrane helices. Transient expression of a ZmALMT1::GFP chimera confirmed that the protein is targeted to the plant cell plasma membrane. We addressed whether ZmALMT1 might underlie the Al-resistance response (i.e. Al-activated citrate exudation) observed in the roots of the Al-tolerant genotype. The physiological, gene expression and functional data from this study confirm that ZmALMT1 is a plasma membrane transporter that is capable of mediating elective anion efflux and influx. However, gene expression data as well as biophysical transport characteristics obtained from Xenopus oocytes expressing ZmALMT1 indicate that this transporter is implicated in the selective transport of anions involved in mineral nutrition and ion homeostasis processes, rather than mediating a specific Al-activated citrate exudation response at the rhizosphere of maize roots.

Review Genetic and molecular mechanisms of aluminum tolerance in plants

“…In contrast, ZmALMT1 (Piñeros et al, 2008) and ZmALMT2 (Ligaba et al, 2012), two members in the ALMT family, were not found to be associated with maize Al tolerance.…”

The ALMT Gene Family Performs Multiple Functions in Plants

“…similarly relies on the ALMT transporter Ma1 which mediates malate accumulation into the vacuoles of developing fruit cells [14]. In maize (Zea mays L.), ZmALMT1 and ZmALMT2 are mainly expressed in root tissues and likely function to assist in balancing charges during nutrient uptake [12,13]. Both proteins localise to the plasma membrane and both are permeable to inorganic anions but ZmALMT2 is also permeable to organic anions as demonstrated by the constitutive release of malate from the roots of transgenic Arabidopsis plants expressing ZmALMT2 [13].…”

“…The characterised ALMT members show a range of functions including Al resistance [1][2][3][4], stomatal function [5][6][7][8][9][10][11], mineral nutrition [12,13,39], microbe interactions [16,17], fruit acidity [14,15], and seed development [18]. Members which have been characterised are widely distributed in higher plant families of Poaceae, Brassicaceae, Fabaceae, Rutaceae, Rosaceae, Vitaceae and Solanaceas (Table 1).…”

“…In maize, ZmALMT1 was initially considered a candidate for an Al resistance gene due to its sequence homology with TaALMT1 [12]. Although ZmALMT1 localises to the plasma membrane, is mainly expressed in root tissue, and shows increased expression with Al treatment, other results indicated that this gene was not involved with the mechanism of Al resistance.…”

“…Although widely spread in plants, relatively little information is available on the roles performed by other members of this family. However those that have been characterised show a range of functions including Al resistance [1][2][3][4], stomatal function [5][6][7][8][9][10][11], mineral nutrition [12,13], fruit acidity [14,15], microbe interactions [16,17] and seed development [18].…”