Copper transporter COPT5 participates in the crosstalk between vacuolar copper and iron pools mobilisation

Àngela Carrió-Seguí,Lola Peñarrubia,Paco Romero,Catherine Curie,Stéphane Mari

doi:10.1038/s41598-018-38005-4

Abstract

Copper (Cu) deficiency affects iron (Fe) homeostasis in several plant processes, including the increased Fe requirements due to cuproprotein substitutions for the corresponding Fe counterpart. Loss-of-function mutants from Arabidopsis thaliana high affinity copper transporter COPT5 and Fe transporters NATURAL RESISTANCE-ASSOCIATED MACROPHAGE PROTEIN 3/4 (NRAMP3 and NRAMP4) were used to study the interaction between metals internal pools. A physiological characterisation showed that the copt5 mutant is sensitive to Fe deficiency, and that nramp3nramp4 mutant growth was severely affected under limiting Cu. By a transcriptomic analysis, we observed that NRAMP4 expression was highly induced in the copt5 mutant under Cu deficiency, while COPT5 was overexpressed in the nramp3nramp4 mutant. As a result, an enhanced mobilisation of the vacuolar Cu or Fe pools, when the other metal export through the tonoplast is impaired in the mutants, has been postulated. However, metals coming from internal pools are not used to accomplish the increased requirements that derive from metalloprotein substitution under metal deficiencies. Instead, the metal concentrations present in aerial parts of the copt5 and nramp3nramp4 mutants conversely show compensated levels of these two metals. Together, our data uncover an interconnection between Cu and Fe vacuolar pools, whose aim is to fulfil interorgan metal translocation.

Highlights

Transition metals copper (Cu) and iron (Fe) are required by organisms to perform a remarkable wide array of functions that are critical for life
The most differentially expressed genes (DEG) were found in the copt[] mutant when grown under Cu deficiency (Fig. 1a,b)
In agreement with the number of DEG shown in the Venn diagrams, the copt[] and WT seedlings grown under optimal control conditions were distributed far from those grown under severe Cu deficiency

Summary

Introduction

Transition metals copper (Cu) and iron (Fe) are required by organisms to perform a remarkable wide array of functions that are critical for life. There is considerable experimental evidence to link the Cu and Fe homeostases at different levels[3,4,5] Among these potential interactions is metalloprotein substitution such as replacement of Arabidopsis Cu/Zn superoxide dismutase (Cu/ZnSOD) with the Fe (FeSOD) counterpart, under Cu scarcity conditions, probably to economise Cu for essential cuproproteins such as plastocyanin[6]. This adjustment is accomplished by the transcription factor PROMOTER BINDING PROTEIN-SQUAMOSA LIKE7 (SPL7)[5,7] and mediated by miR398 that regulates CSD1 and CSD2 genes that respectively encode cytosolic and chloroplastic Cu/ZnSODs8. Under Fe deficiency, the FeSOD is replaced with the Cu/ZnSOD as Fe down-regulates miR3984 Another interaction is metal competition for ligands in long-distance traffic[9]. A genetic screen showed that the vit[1] mutation suppresses the nramp3nramp[4] phenotype, which illustrates the plasticity of Fe storage in Arabidopsis embryos[21]

Methods

Results

Conclusion