Physiological Importance of Molybdate Transporter Family 1 in Feeding the Molybdenum Cofactor Biosynthesis Pathway in Arabidopsis thaliana

Abstract

Molybdate uptake and molybdenum cofactor (Moco) biosynthesis were investigated in detail in the last few decades. The present study critically reviews our present knowledge about eukaryotic molybdate transporters (MOT) and focuses on the model plant Arabidopsis thaliana, complementing it with new experiments, filling missing gaps, and clarifying contradictory results in the literature. Two molybdate transporters, MOT1.1 and MOT1.2, are known in Arabidopsis, but their importance for sufficient molybdate supply to Moco biosynthesis remains unclear. For a better understanding of their physiological functions in molybdate homeostasis, we studied the impact of mot1.1 and mot1.2 knock-out mutants, including a double knock-out on molybdate uptake and Moco-dependent enzyme activity, MOT localisation, and protein–protein interactions. The outcome illustrates different physiological roles for Moco biosynthesis: MOT1.1 is plasma membrane located and its function lies in the efficient absorption of molybdate from soil and its distribution throughout the plant. However, MOT1.1 is not involved in leaf cell imports of molybdate and has no interaction with proteins of the Moco biosynthesis complex. In contrast, the tonoplast-localised transporter MOT1.2 exports molybdate stored in the vacuole and makes it available for re-localisation during senescence. It also supplies the Moco biosynthesis complex with molybdate by direct interaction with molybdenum insertase Cnx1 for controlled and safe sequestering.

The Mechanisms of Molybdate Distribution and Homeostasis with Special Focus on the Model Plant Arabidopsis thaliana

“…The complexity of molybdate homeostasis in a multicellular organism forced evolutions of A. thaliana to develop mechanisms for micro-compartmentation, safekeeping, and allocation. For all these tasks, the six identified molybdate transporters have to be highly molybdate-specific; otherwise, a precise molybdate homeostasis would be impossible [ 65 ]. These six MOTs were categorized in two independent MOT families ( Figure 3 ) [ 16 , 66 ].…”

The History of the Molybdenum Cofactor—A Personal View

“…In plants, after synthesis of the MPT moiety, the chemical backbone is built for binding and coordinating the Mo atom. Mo is taken up into the cell in the form of molybdate, which is facilitated by high-affinity transport systems (reviewed by Minner-Meinen et al [ 111 ] in this Special Issue). As described above in the paragraph “High molybdate repair”, molybdate-repairable mutants have been known for a long time: Aspergillus CnxE [ 63 ], Neurospora nit–9ABC [ 112 , 113 ], and tobacco CnxA [ 40 ].…”

“…Furthermore, Cnx1 also makes protein–protein contact with the molybdate transporter in the living cell. Details are summarized in the paper by Minner-Meinen et al [ 111 ] in this Special Issue.…”

“…Molybdate for this reaction is supplied by the vacuolar exporter Mot2 (a Mot2-mutant leads to a shortage of molybdate in the cytosol and the accumulation of molybdate in the vacuole) [ 146 ]. Later, Mot2 was renamed as Mot1.2 [ 111 ]. The Mot1-transporter is the cellular Mo-importer and resides in the plasma membrane [ 111 ].…”

“…Later, Mot2 was renamed as Mot1.2 [ 111 ]. The Mot1-transporter is the cellular Mo-importer and resides in the plasma membrane [ 111 ]. Mature Moco can be either bound to a Moco-binding protein (MoBP) or directly to the Mo enzymes.…”