Manganese in Plants: From Acquisition to Subcellular Allocation

Abstract

Manganese (Mn) is an important micronutrient for plant growth and development and sustains metabolic roles within different plant cell compartments. The metal is an essential cofactor for the oxygen-evolving complex (OEC) of the photosynthetic machinery, catalyzing the water-splitting reaction in photosystem II (PSII). Despite the importance of Mn for photosynthesis and other processes, the physiological relevance of Mn uptake and compartmentation in plants has been underrated. The subcellular Mn homeostasis to maintain compartmented Mn-dependent metabolic processes like glycosylation, ROS scavenging, and photosynthesis is mediated by a multitude of transport proteins from diverse gene families. However, Mn homeostasis may be disturbed under suboptimal or excessive Mn availability. Mn deficiency is a serious, widespread plant nutritional disorder in dry, well-aerated and calcareous soils, as well as in soils containing high amounts of organic matter, where bio-availability of Mn can decrease far below the level that is required for normal plant growth. By contrast, Mn toxicity occurs on poorly drained and acidic soils in which high amounts of Mn are rendered available. Consequently, plants have evolved mechanisms to tightly regulate Mn uptake, trafficking, and storage. This review provides a comprehensive overview, with a focus on recent advances, on the multiple functions of transporters involved in Mn homeostasis, as well as their regulatory mechanisms in the plant's response to different conditions of Mn availability.

Keywords: Arabidopsis; barley; intracellular distribution; manganese deficiency; manganese toxicity; manganese transport; manganese uptake; rice.

FIGURE 1

Tissue specificity and subcellular localization of Mn transport proteins in roots of different plant species. (A) Mn transport proteins in epidermis, endodermis, cortex, and stele (including pericycle) of Arabidopsis roots. (B) Mn transport proteins in exodermis, endodermis, and stele of rice roots. Radial transport of Mn²⁺ is carried out by OsNRAMP5 and OsMTP9, which are polarly localized transporters at both the exodermis and the endodermis, providing a unidirectional flux of Mn from the soil to the stele (indicated as dashed arrow). (C) Mn transport proteins in epidermis, endodermis, cortex, and stele of roots of other plant species. (A–C) White arrows indicate import into the cytosol, black arrows indicate export out of the cytosol. Transport proteins with yet unknown root tissue specificity are marked by asterisks. Proteins which subcellular localization only shown in yeast but not in plants are indicated by a question mark. Hv, Hordeum vulgare; Pt, Populus trichocarpa; Sh, Stylosanthes hamata; Ta, Triticum aestivum; Vv, Vitis vinifera.

FIGURE 2

Expression of genes encoding Mn transport proteins in aerial parts of Arabidopsis and rice. (A) Mn transport proteins in shoots of Arabidopsis. Transporters listed on the left are expressed in the vasculature of leaves, transporters listed on the right are expressed throughout the above-ground tissues of the plant. In vegetative tissues, AtVIT1 is only expressed in cotyledons. (B) Mn transport proteins in shoots of rice. OsMTP11 and OsYSL2 are expressed in the vasculature. OsNRAMP3 is expressed in the first node (orange). OsYSL6 and OsMTP8.1/2 are expressed in older leaves, whereas expression of OsVIT1/2 is more pronounced in younger leaves.

FIGURE 3

Subcellular localization of Mn transport proteins in aerial parts of different plant species. (A) Arabidopsis, (B) rice, and (C) other species. White arrows represent import into the cytosol, black arrows represent export from the cytosol. Transport pathways with uncharacterized Mn transporters are indicated by a question mark. Hv, Hordeum vulgare; Le, Lycopersicum esculentum (syn. Solanum lycopersicum); Pt, Populus trichocarpa; Sh, Stylosanthes hamata; Ta, Triticum aestivum; Vv, Vitis vinifera.