Abstract
Tungsten (W) finds increasing application in military, aviation and household appliance industry, opening new paths into the environment. Since W shares certain chemical properties with the essential plant micronutrient molybdenum (Mo), it is proposed to inhibit enzymatic activity of molybdoenzymes [e.g., nitrate reductase (NR)] by replacing the Mo-ion bound to the co-factor. Recent studies suggest that W, much like other heavy metals, also exerts toxicity on its own. To create a comprehensive picture of tungsten stress, this study investigated the effects of W on growth and metabolism of soybean (Glycine max), depending on plant nitrogen regime [nitrate fed (N fed) vs. symbiotic N2 fixation (N fix)] by combining plant physiological data (biomass production, starch and nutrient content, N2 fixation, nitrate reductase activity) with root and nodule proteome data. Irrespective of N regime, NR activity and total N decreased with increasing W concentrations. Nodulation and therefore also N2 fixation strongly declined at high W concentrations, particularly in N fix plants. However, N2 fixation rate (g N fixed g−1 nodule dwt) remained unaffected by increasing W concentrations. Proteomic analysis revealed a strong decline in leghemoglobin and nitrogenase precursor levels (NifD), as well as an increase in abundance of proteins involved in secondary metabolism in N fix nodules. Taken together this indicates that, in contrast to the reported direct inhibition of NR, N2 fixation appears to be indirectly inhibited by a decrease in nitrogenase synthesis due to W induced changes in nodule oxygen levels of N fix plants. Besides N metabolism, plants exhibited a strong reduction of shoot (both N regimes) and root (N fed only) biomass, an imbalance in nutrient levels and a failure of carbon metabolic pathways accompanied by an accumulation of starch at high tungsten concentrations, independent of N-regime. Proteomic data (available via ProteomeXchange with identifier PXD010877) demonstrated that the response to high W concentrations was independent of nodule functionality and dominated by several peroxidases and other general stress related proteins. Based on an evaluation of several W responsive proteotypic peptides, we identified a set of protein markers of W stress and possible targets for improved stress tolerance.
Highlights
Increasing environmental contamination with heavy metals and other xenobiotics has become a major concern for agricultural production and human food safety
The W induced decrease in shoot biomass production of nitrate fed (N fed) plants shows a similar decline as observed for N2 fixation (N fix) plants, N fed plants exhibited a significantly higher initial biomass for controls and throughout all tungsten treatments
Root:shoot ratio showed a significant increase in N fix plants with increasing tungsten concentrations but did not significantly increase in the N fed treatment (Table S1)
Summary
Increasing environmental contamination with heavy metals and other xenobiotics has become a major concern for agricultural production and human food safety. Despite the myriad of applications tungsten finds in different industries, ranging from everyday household appliances to high tech and military products, the transition metal W has received only little attention, and information about the behavior of tungsten in the plant-soil environment is limited. Besides discharge of W utilizing industries and W mining sites, tungsten finds entry into the environment due to disposal of W-containing products, military activities, coal driven power plants and soil fertilizer application (Koutsospyros et al, 2006; Strigul et al, 2010). Tungsten concentrations in soils from abandoned mining sites in Portugal are reported to range from 0.8 to 684 mg kg−1(Pratas et al, 2005). At least in its unpolymerized form, to be readily taken up by plants to other anions (Schwarz et al, 2007; Bevers et al, 2009)
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