Advances in the Mechanisms of Plant Tolerance to Manganese Toxicity

Abstract

Manganese (Mn) is an essential element for plant growth due to its participation in a series of physiological and metabolic processes. Mn is also considered a heavy metal that causes phytotoxicity when present in excess, disrupting photosynthesis and enzyme activity in plants. Thus, Mn toxicity is a major constraint limiting plant growth and production, especially in acid soils. To cope with Mn toxicity, plants have evolved a wide range of adaptive strategies to improve their growth under this stress. Mn tolerance mechanisms include activation of the antioxidant system, regulation of Mn uptake and homeostasis, and compartmentalization of Mn into subcellular compartments (e.g., vacuoles, endoplasmic reticulum, Golgi apparatus, and cell walls). In this regard, numerous genes are involved in specific pathways controlling Mn detoxification. Here, we summarize the recent advances in the mechanisms of Mn toxicity tolerance in plants and highlight the roles of genes responsible for Mn uptake, translocation, and distribution, contributing to Mn detoxification. We hope this review will provide a comprehensive understanding of the adaptive strategies of plants to Mn toxicity through gene regulation, which will aid in breeding crop varieties with Mn tolerance via genetic improvement approaches, enhancing the yield and quality of crops.

Keywords: Mn detoxification; gene function; manganese toxicity; subcellular compartment; tolerance mechanism.

Figure 1

Schematic representation of Mn toxicity and strategies for increasing Mn tolerance in plants. Mn toxicity can trigger oxidative stress and disrupt photosynthesis, which may result in the generation of interveinal chlorosis in young leaves, necrotic dark spots on mature leaves, and crinkled leaf. Furthermore, Mn toxicity can lead to the formation of brown roots and prevent the uptake and translocation of other mineral elements. In plants, Mn tolerance strategies include modification of Mn translocation and distribution, sequestration of Mn into subcellular compartments, modulation of the antioxidant system, changes in biochemical pathways, and regulation of Mn transporters. In addition, the mediation of root exudates, the application of Si in roots, and the amelioration of soil acidification, humidity, and organic matter content also contribute to increase plant Mn tolerance. Red arrows indicate the toxic effects of excess Mn to plants. Purple arrows represent the adaptive strategies of plants to Mn toxicity.

Figure 2

Summary of genes affecting Mn transport and tolerance in plants. Squares: Import into the cytosol; circles: Export out of the cytosol; blue: MTP family; green: ZTP family; red: Nramp family; purple: YSL family; yellow: IRT family; orange: ECA family; cyan: CAX family; brown: DMT family; gray: unknown. ER: Endoplasmic reticulum; Nramp: Natural resistance-associated macrophage protein; MTP: Metal tolerance protein; DMT: Divalent metal transporter; ZIP/IRT: Zinc-regulated transporter/iron-regulated transporter-like proteins; YSL: Yellow stripe-like protein; CAX: Cation exchanger; ECAs: ER-type calcium ATPases; MDH: Malate dehydrogenase; ALMT: Aluminum-activated malate transporter; OAA: Oxaloacetate; ROS: Reactive oxygen species; SOD: Superoxide dismutase; POD: Peroxidase; CAT: Catalase. At: Arabidopsis thaliana; Os: Oryza sativa; Gm: Glycine max; Hv: Hordeum vulgare; Mt: Medicago tvuncatula; Cs: Cucumis sativus; Sh: Stylosanthes hamata; Sg: Stylosanthes guianensis; Le: Lycopersicon esculentum; Bm: Beta vulgaris subspecies maritima; Pt: Populus trichocarpa. Question marks behind some genes mean that the exact roles of these genes or their localizations remain to be further clarified.