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Synchrotron-Based Techniques Shed Light on Mechanisms of Plant Sensitivity and Tolerance to High Manganese in the Root Environment
Blamey, P., M. Hernandez-Soriano, M. Cheng, C. Tang, D. Paterson, E. Lombi, W. Wang, K. Scheckel, AND P. Kopittke. Synchrotron-Based Techniques Shed Light on Mechanisms of Plant Sensitivity and Tolerance to High Manganese in the Root Environment. Michael R. Blatt (ed.), PLANT PHYSIOLOGY. American Society of Plant Biologists, Rockville, MD, 169(3):2006-2020, (2015).
Manganese (Mn) is an essential element for plant growth, but its availability differs greatly in space and time, depending largely on the nature and amount of Mn minerals present and on the soil’s pH and redox potential. With an elaborate chemistry, Mn forms complexes with many organic and inorganic ligands. In soils, Mn has three common oxidation states, Mn(II), Mn(III), and Mn(IV), which form hydrated oxides of mixed valency; Mn is present also as numerous carbonates, silicates, sulfates, and phosphates (Lindsay, 1979). Cationic Mn2+ is the most common form readily absorbed by plant roots (Clarkson,1988). Decreased plant growth due to Mn deficiency occurs mostly in alkaline soils but also in highly-weathered soils low in Mn. In contrast, Mn toxicity occurs in acid or waterlogged soils high in Mn minerals. Microbial activity is important in the oxidation and reduction of Mn in soils, resulting in temporal changes in Mn availability. The present study aimed to determine the distribution and speciation of Mn in fresh roots, stems, and leaves of four crop species, soybean, white lupin (Lupinus albus), narrow-leafed lupin (Lupinus angustifolius), and sunflower, which differ in tolerance to high Mn. It was hypothesized that Mn distribution and speciation would differ between Mn-sensitive soybean and the three other species. Furthermore, we considered it likely that the Mn tolerance mechanism of sunflower would differ from those of the two lupin species, which do not have darkened trichomes when grown at high Mn.
Plant species differ in response to high available manganese (Mn), but the mechanisms of sensitivity and tolerance are poorly understood. In solution culture, greater than or equal to 30 µM Mn decreased the growth of soybean (Glycine max), but white lupin (Lupinus albus), narrow-leafed lupin (Lupin angustifolius), and sunflower (Helianthus annuus) grew well at 100 µM Mn. Differences in species’ tolerance to high Mn could not be explained simply by differences in root, stem, or leaf Mn status, being 8.6, 17.1, 6.8, and 9.5 mmol kg-1 leaf fresh mass at 100 µM Mn. Furthermore, x-ray absorption near edge structure analyses identified the predominance of Mn(II), bound mostly to malate or citrate, in roots and stems of all four species. Rather, differences in tolerance were due to variations in Mn distribution and speciation within leaves. In Mn-sensitive soybean, in situ analysis of fresh leaves using x-ray fluorescence microscopy combined with x-ray absorption near edge structure showed high Mn in the veins, and manganite [Mn(III)] accumulated in necrotic lesions apparently through low Mn sequestration in vacuoles or other vesicles. In the two lupin species, most Mn accumulated in vacuoles as either soluble Mn(II) malate or citrate. In sunflower, Mn was sequestered as manganite at the base of nonglandular trichomes. Hence, tolerance to high Mn was ascribed to effective sinks for Mn in leaves, as Mn(II) within vacuoles or through oxidation of Mn(II) to Mn(III) in trichomes. These two mechanisms prevented Mn accumulation in the cytoplasm and apoplast, thereby ensuring tolerance to high Mn in the root environment.