Abstract
Manganese is an essential micronutrient for plant growth but can be toxic to plants when it reaches excessive levels. Although metal tolerance proteins (MTPs), which belong to the cation diffusion facilitator (CDF) family, have been demonstrated to play critical roles in manganese (Mn) tolerance in plants, the characteristics and functions of GmMTP members in the response of soybean (Glycine max) to Mn toxicity have not been documented. In this study, growth inhibition was observed in soybean plants that were exposed to a toxic level of Mn in hydroponics, as reflected by the generation of brown spots, and decreased leaf chlorophyll concentration and plant fresh weight. Subsequent genome-wide analysis resulted in the identification of a total of 14 GmMTP genes in the soybean genome. Among these GmMTPs, 9 and 12 were found to be regulated by excess Mn in leaves and roots, respectively. Furthermore, the function of GmMTP8.1, a Mn-CDF homologue of ShMTP8 identified in the legume Stylosanthes hamata that is involved in Mn detoxification, was characterized. Subcellular localization analysis showed that GmMTP8.1 was localized to the endoplasmic reticulum (ER). Heterologous expression of GmMTP8.1 led to the restoration of growth of the Mn-hypersensitive yeast (Saccharomyces cerevisiae) mutant Δpmr1, which is made defective in Mn transport into the Golgi apparatus by P-type Ca/Mn-ATPase. Furthermore, GmMTP8.1 overexpression conferred tolerance to the toxic level of Mn in Arabidopsis (Arabidopsis thaliana). Under excess Mn conditions, concentrations of Mn in shoots but not roots were decreased in transgenic Arabidopsis, overexpressing GmMTP8.1 compared to the wild type. The overexpression of GmMTP8.1 also led to the upregulation of several transporter genes responsible for Mn efflux and sequestration in Arabidopsis, such as AtMTP8/11. Taken together, these results suggest that GmMTP8.1 is an ER-localized Mn transporter contributing to confer Mn tolerance by stimulating the export of Mn out of leaf cells and increasing the sequestration of Mn into intracellular compartments.
Highlights
As one of the essential micronutrients for plant growth, manganese (Mn) acts as an activator of many enzymes, serving various functions in a set of physiological and biochemical processes (Millaleo et al, 2010; Marschner, 2012; Long et al, 2021)
The results showed that excess Mn treatments (50 and 100 μM) resulted in the generation of brown spots on mature leaves compared to the control (5 μM Mn) (Figure 1A)
The results showed that the green fluorescent protein (GFP) signal of GmMTP8.1 was found to be co-localized with that of the endoplasmic reticulum (ER) marker but not localized in the tonoplast of tobacco leaf epidermal cells, whereas the fluorescence of cells transformed with GFP alone was observed in whole cells, such as plasma membrane, cytoplasm, and nucleus (Figures 6A,B)
Summary
As one of the essential micronutrients for plant growth, manganese (Mn) acts as an activator of many enzymes, serving various functions in a set of physiological and biochemical processes (Millaleo et al, 2010; Marschner, 2012; Long et al, 2021). Mn is required by plants at a low dose and can cause phytotoxicity when present in excess (Millaleo et al, 2010; Shao et al, 2017). Mn toxicity is an important factor limiting plant growth on acid, poorly drained soils, and sterilized soils. Mn toxicity inhibits enzyme activity, declines chlorophyll biosynthesis and photosynthesis, and impairs the uptake and translocation of other mineral elements (Fernando and Lynch, 2015; Li et al, 2019). Better understanding of mechanisms underlying the response of plants to Mn toxicity is of great importance for breeding Mn-tolerant crop varieties
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