Abstract
Sugar maple and red maple are closely-related co-occurring tree species significant to the North American forest biome. Plant abiotic stress effects including nutritional imbalance and manganese (Mn) toxicity are well documented within this system, and are implicated in enhanced susceptibility to biotic stresses such as insect attack. Both tree species are known to overaccumulate foliar manganese (Mn) when growing on unbuffered acidified soils, however, sugar maple is Mn-sensitive, while red maple is not. Currently there is no knowledge about the cellular sequestration of Mn and other nutrients in these two species. Here, electron-probe x-ray microanalysis was employed to examine cellular and sub-cellular deposition of excessively accumulated foliar Mn and other mineral nutrients in vivo. For both species, excess foliar Mn was deposited in symplastic cellular compartments. There were striking between-species differences in Mn, magnesium (Mg), sulphur (S) and calcium (Ca) distribution patterns. Unusually, Mn was highly co-localised with Mg in mesophyll cells of red maple only. The known sensitivity of sugar maple to excess Mn is likely linked to Mg deficiency in the leaf mesophyll. There was strong evidence that Mn toxicity in sugar maple is primarily a symplastic process. For each species, leaf-surface damage due to biotic stress including insect herbivory was compared between sites with acidified and non-acidified soils. Although it was greatest overall in red maple, there was no difference in biotic stress damage to red maple leaves between acidified and non-acidified soils. Sugar maple trees on buffered non-acidified soil were less damaged by biotic stress compared to those on unbuffered acidified soil, where they are also affected by Mn toxicity abiotic stress. This study concluded that foliar nutrient distribution in symplastic compartments is a determinant of Mn sensitivity, and that Mn stress hinders plant resistance to biotic stress.
Highlights
The essential trace element manganese (Mn) is integral to photosynthesis, free radical mitigation and redox processes, yet certain conditions of soil chemistry, climate and/or genetic predisposition can render it toxic to plants [1]
Uppermost canopy leaves maximally exposed to sunlight were targeted because visible and UV radiation generate reactive oxygen species (ROS) that cause oxidative stress exacerbated by excess foliar Mn [13, 23] As detailed below, leaf material was sampled for the purposes of bulk-tissue chemical analysis, image analysis, light microscopy (LM), transmission electron microscopy (TEM), and scanning electron microscopy energy dispersive spectroscopy (SEM EDS)
Leaf chemical analyses by ICP obtained here confirmed existing knowledge about the nutritional status of sugar maple and red maple trees at this and other sites on the Allegheny Plateau, i.e. that both tree species on unbuffered acidified soils upslope accumulate much higher foliar-Mn concentrations than they do on buffered soils downslope (Table 1)
Summary
The essential trace element manganese (Mn) is integral to photosynthesis, free radical mitigation and redox processes, yet certain conditions of soil chemistry, climate and/or genetic predisposition can render it toxic to plants [1]. Minor shifts in soil chemistry and/or climatic conditions can enhance soil-Mn bioavailability to levels potentially deleterious to plants [7,8,9,10,11,12,13,14]. Soil Mn concentrations coupled with seasonal variation in rainfall and temperature have a strong bearing on plant over-exposure to Mn(II), while genetics largely determines the uptake of and physiological response to high shoot-tissue Mn concentrations. The enhanced solubilisation of soil-Mn triggers nutritional deficiencies since Mn(II) outcompetes similar ions such as Ca(II) and Mg(II) for plant uptake. Given that the manifestation and extent of Mn phytotoxicity as observed in the field largely hinges on climatic variables, stress symptoms commonly are seasonally heterogeneous
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