The Biochemical Properties of Manganese in Plants

Abstract

Manganese (Mn) is an essential micronutrient with many functional roles in plant metabolism. Manganese acts as an activator and co-factor of hundreds of metalloenzymes in plants. Because of its ability to readily change oxidation state in biological systems, Mn plays and important role in a broad range of enzyme-catalyzed reactions, including redox reactions, phosphorylation, decarboxylation, and hydrolysis. Manganese(II) is the prevalent oxidation state of Mn in plants and exhibits fast ligand exchange kinetics, which means that Mn can often be substituted by other metal ions, such as Mg(II), which has similar ion characteristics and requirements to the ligand environment of the metal binding sites. Knowledge of the molecular mechanisms catalyzed by Mn and regulation of Mn insertion into the active site of Mn-dependent enzymes, in the presence of other metals, is gradually evolving. This review presents an overview of the chemistry and biochemistry of Mn in plants, including an updated list of known Mn-dependent enzymes, together with enzymes where Mn has been shown to exchange with other metal ions. Furthermore, the current knowledge of the structure and functional role of the three most well characterized Mn-containing metalloenzymes in plants; the oxygen evolving complex of photosystem II, Mn superoxide dismutase, and oxalate oxidase is summarized.

Keywords: Manganese; Mn cluster; catalysis; database; enzyme; metalloenzyme; oxalate oxidase; photosystem II; superoxide dismutase.

Figure 1

(a) The three dominating coordination geometries and coordination numbers observed in Mn (purple sphere) containing metalloproteins are tetrahedral (Td, n = 4); trigonal bipyramidal (TBp, n = 5) and octahedral (Oh, n = 6). (b) The active site of Mn-SOD in the presence of Mn (purple sphere), with and without water molecules (W1 and W2, red spheres) in the coordinating sphere. Three His residues (His 165, 27, and 81), one Asp (161) coordinates Mn, and the involvement of 0, 1, or 2 water molecules determines the geometry of the Mn complex at the active site. Zero water produces Td, binding of W1 yields TBp, and binding of W1 and W2 produces the Oh geometry. It has been speculated that the geometry of the active sites changes during scavenging of reactive oxygen species [22].

Figure 2

Distribution of Mn activated enzymes across the six Enzyme Commission (EC) classes together with the relative frequencies (%) of the coordinated metal ion for each EC class. A total of 101distinct Mn activated enzymes is described in the UniProt Knowledgebase for Arabidopsis thaliana, when filtered by reviewed records, accessible cofactor information, and protein name. Of these enzymes, 37 exclusively contain Mn as a cofactor, 44 enzymes are activated by either Mn or Mg, while 20 enzymes are reported to coordinate with Mn, Mg, or other divalent metals (Ca, Zn, Fe, Co, Ni, Cu).

Figure 3

(a) The Kok cycle showing the steps of oxygen evolution in the oxygen evolving complex (OEC) of photosystem II (PSII) with details of the S_i states (S₀–S₄), the light induced oxidation steps of electron (e⁻) and proton (H⁺) release, together with the uptake of two molecules of H₂O, which can be summarized to: $2{\mathrm{H}}_2\mathrm{O} \to 4{\mathrm{H}}^{+}+4{ \mathrm{e}}^{-} +{\mathrm{O}}_2$. (b) The chemical structure shows the configuration and position of the metal atoms in the Mn4Ca cluster, resembling a distorted chair-like form. The distorted seat base is formed by three Mn and one Ca atoms in a cubane structure, and the back is formed by the fourth Mn (Mn4), the so-called dangler Mn, which lies outside the cubane, and has been proposed to act as the site of catalysis.