AtIREG2 Encodes a Tonoplast Transport Protein Involved in Iron-dependent Nickel Detoxification in Arabidopsis thaliana Roots

Abstract

Iron acquisition in Arabidopsis depends mainly on AtIRT1, a Fe 2؉ transporter in the plasma membrane of root cells. However, substrate specificity of AtIRT1 is low, leading to an excess accumulation of other transition metals in iron-deficient plants.In the present study we describe AtIREG2 as a nickel transporter at the vacuolar membrane that counterbalances the low substrate specificity of AtIRT1 and possibly other iron transport systems in iron-deficient root cells. showed an increased tolerance to elevated concentrations of nickel, whereas T-DNA insertion lines lacking AtIREG2 expression were more sensitive to nickel, particularly under iron deficiency, and accumulated less nickel in roots. We therefore propose a role of AtIREG2 in vacuolar loading of nickel under iron deficiency and thus identify it as a novel component in the iron deficiency stress response.Iron deficiency in plants is visually expressed as chlorosis, first appearing in the youngest developing leaves and accompanied by a reduction in growth rate, dry matter production, and in most cases by a decrease of iron concentration (1). At the same time, root uptake capacities and leaf concentrations of other divalent metal cations increase (2, 3). In soils or nutrient solutions with unbalanced microelement supply, iron deficiency can then promote the toxicity of other transition metals (4, 5). Such toxicity seems also to be the case with nickel, supported by the observation that phytotoxicity of nickel decreased with increasing iron:nickel ratios in the leaf tissue (6, 7). Thus, an increased sensitivity to heavy metals under iron deficiency might represent a secondary, growth-limiting factor besides the lack of iron itself.Molecular studies in yeast showed that an iron deficiencyinduced accumulation of transition metals other than iron was explained by a higher activity of non-selective low affinity iron transport. Deletion of FET3, an essential component for high affinity iron uptake in yeast, leads to a constitutive iron-deficient phenotype and a concomitant up-regulation of FET4, which encodes a low affinity Fe(II) transporter with poor substrate selectivity (8). As a consequence, sensitivity to elevated concentrations of the transition metals cobalt, copper, zinc, and manganese was higher in fet3 mutants than in the corresponding wild type, consistent with increased metal accumulation (8).In Arabidopsis, iron-dependent overaccumulation of divalent metal cations was found to be mediated by the Fe(II) transporter AtIRT1, which in fact transports a broad range of transition metals (9). Atirt1 T-DNA insertion lines no longer accumulated manganese, zinc, and cobalt under iron deficiency and even showed an increased tolerance to toxic levels of cadmium (10). Thus, accumulation of certain transition metals in iron-deficient Arabidopsis plants directly depends on AtIRT1 and appears as an unavoidable side effect of iron deficiencyinduced iron acquisition.In the search for genes that might be involved in metal transport in Arabidopsis roots, homology to ...

Multiple Antibiotic Resistance in Arabidopsis Is Conferred by Mutations in a Chloroplast-Localized Transport Protein

“…This up-regulation leads to an increase in cytoplasmic iron, but due to the poor substrate specificity of IRT1, it also results in increasing cytoplasmic levels of other toxic divalent metal cations, such as nickel. One of the MAR1 homologs in Arabidopsis, AtIREG2, is proposed to play a role in the vacuolar sequestration of excess nickel accumulated under iron-limiting conditions due to the action of IRT1 (Schaaf et al, 2006). Schaaf et al showed that AtIREG2 was up-regulated under iron deficiency, in contrast to MAR1, which is down-regulated (Fig.…”

“…Thus, we suggest that MAR1 and AtIREG2 play distinct roles in the plant cell. Their expression patterns are quite different: AtIREG2 is mainly expressed in the root (Schaaf et al, 2006), while MAR1 is highly expressed in all tissues (Supplemental Fig. S4C).…”

“…S4C). AtIREG2 localizes to the vacuole (Schaaf et al, 2006), while MAR1 localizes to the chloroplast (Fig. 4).…”

“…2A), which is annotated as having low similarity to ferroportin1 from Danio rerio. At5g26820 has been described as AtIREG3 based on sequence similarity to AtIREG1 and AtIREG2, two iron-regulated transporters in Arabidopsis (Schaaf et al, 2006). More recently, it has been described as RTS3, and two mutations in the gene (rts3-1 and rts3-2; Fig.…”

“…One of the MAR1 homologs in Arabidopsis, AtIREG2, was found to be up-regulated under iron deficiency (Schaaf et al, 2006). With this in mind, we examined MAR1 for transcriptional changes under iron limita- , and a merge of the two channels (D, H, L, and P) are included for each protoplast.…”