Variation in Molybdenum Content Across Broadly Distributed Populations of Arabidopsis thaliana Is Controlled by a Mitochondrial Molybdenum Transporter (MOT1)

Abstract

Molybdenum (Mo) is an essential micronutrient for plants, serving as a cofactor for enzymes involved in nitrate assimilation, sulfite detoxification, abscisic acid biosynthesis, and purine degradation. Here we show that natural variation in shoot Mo content across 92 Arabidopsis thaliana accessions is controlled by variation in a mitochondrially localized transporter (Molybdenum Transporter 1 - MOT1) that belongs to the sulfate transporter superfamily. A deletion in the MOT1 promoter is strongly associated with low shoot Mo, occurring in seven of the accessions with the lowest shoot content of Mo. Consistent with the low Mo phenotype, MOT1 expression in low Mo accessions is reduced. Reciprocal grafting experiments demonstrate that the roots of Ler-0 are responsible for the low Mo accumulation in shoot, and GUS localization demonstrates that MOT1 is expressed strongly in the roots. MOT1 contains an N-terminal mitochondrial targeting sequence and expression of MOT1 tagged with GFP in protoplasts and transgenic plants, establishing the mitochondrial localization of this protein. Furthermore, expression of MOT1 specifically enhances Mo accumulation in yeast by 5-fold, consistent with MOT1 functioning as a molybdate transporter. This work provides the first molecular insight into the processes that regulate Mo accumulation in plants and shows that novel loci can be detected by association mapping. Plants must acquire all the mineral nutrients they require for survival from the complex chemical and biological environment of the soil. A better understanding of the way plants do this would not only allow improvements in sustainable agricultural productivity, but could also improve human health through enhancement of the nutritional quality of foods. One such essential mineral nutrient required by plants is molybdenum (Mo), which is needed as a cofactor in several critical biochemical reactions, including the utilization of nitrogen from the soil. By searching through numerous natural populations of Arabidopsis thaliana (Arabidopsis), we were able to identify a DNA deletion that drives the natural variation in Mo accumulation observed in these populations. This deletion reduces expression of a gene (MOT1) that the authors establish to encode a mitochondrially localized molybdenum transporter. Loss of expression of MOT1 in the roots of Arabidopsis causes a significant reduction in whole plant Mo accumulation, though the mechanism by which this Mo transporter regulates whole plant Mo from the mitochondria remains to be established.