Molybdenum metabolism in plants and crosstalk to iron

Abstract

In the form of molybdate the transition metal molybdenum is essential for plants as it is required by a number of enzymes that catalyze key reactions in nitrogen assimilation, purine degradation, phytohormone synthesis, and sulfite detoxification. However, molybdate itself is biologically inactive and needs to be complexed by a specific organic pterin in order to serve as a permanently bound prosthetic group, the molybdenum cofactor, for the socalled molybdo-enyzmes. While the synthesis of molybdenum cofactor has been intensively studied, only little is known about the uptake of molybdate by the roots, its transport to the shoot and its allocation and storage within the cell. Yet, recent evidence indicates that intracellular molybdate levels are tightly controlled by molybdate transporters, in particular during plant development. Moreover, a tight connection between molybdenum and iron metabolisms is presumed because (i) uptake mechanisms for molybdate and iron affect each other, (ii) most molybdo-enzymes do also require iron-containing redox groups such as iron-sulfur clusters or heme, (iii) molybdenum metabolism has recruited mechanisms typical for iron-sulfur cluster synthesis, and (iv) both molybdenum cofactor synthesis and extramitochondrial iron-sulfur proteins involve the function of a specific mitochondrial ABC-type transporter.

Keywords: aldehyde oxidase; iron; molybdate transporter; molybdenum; molybdo-enzymes; nitrate reductase; sulfite oxidase; xanthine dehydrogenase.

FIGURE 1

Molybdenum metabolism in higher plant cells. The main components of molybdenum metabolism in plants are shown including the Moco biosynthetic pathway (CNX proteins) in mitochondria and cytosol, the Moco user enzymes and their respective main functions in nitrogen assimilation (NR), ABA synthesis (AAO3), purine catabolism (XDH1), and sulfite detoxification (SO). mARC enzymes are proposed to function in reduction of certain N-hydroxylated substrates, which have not yet been identified. While one of the two mARC isoforms (mARC2) contains an NH₂-terminal mitochondrial targeting sequence, such targeting sequence is absent at the second isoform, which therefore is assumed to act in the cytosol. In contrast to the molybdate transporter MOT2, which functions at the vacuolar membrane as a molybdate exporter, MOT1 might localize to the endomembrane system, possibly to the endoplasmic reticulum. A mitochondrial localization of MOT1 has also been reported but appears less likely as no obvious reason exists for import or export of molybdate into or out of the mitochondria, respectively. The plant homolog (MFS-MOT) of the major facilitator superfamily molybdate transporter MOT2 from Chlamydomonas might be required for molybdate import across the plasma membrane. The function of the Moco sulfurase ABA3 in activation of AO and XDH is indicated, just as the functions of the mitochondrial ABC transporter ATM3 in export of cPMP from mitochondria and in cytosolic iron-sulfur cluster ([Fe-S]) assembly for AO and XDH (and other extra-mitochondrial proteins). Further details are given in the main text and are reviewed by Bittner and Mendel (2010) and Mendel (2013). Molybdo-enzymes are indicated by blue letters, other components of molybdenum metabolism by orange letters; dotted arrows indicate requirement for Moco by molybdo-enzymes.