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PREMISE: The ecological implications of hyperaccumulation have been investigated at the organismal level, but are poorly understood at the plant community level. Questions addressed here were: Does the presence of selenium (Se) hyperaccumulators affect Se distribution and concentration in their native soil, and do hyperaccumulators affect overall vegetation properties and species composition? METHODS: Plant survey and soil Se mapping were performed at three seleniferous sites in Colorado. In season one, plots with and without hyperaccumulators were compared for (1) bare ground, canopy cover, and species richness; (2) relative species abundance; (3) soil Se distribution and concentration. In season two, a smaller-scale design was implemented, focusing on areas 3 m in diameter around hyperaccumulators versus nonhyperaccumulators in 44 paired plots on one site. RESULTS: Plots with hyperaccumulators generally showed more bare ground, less canopy cover, higher species richness, and 2-3-fold higher soil Se levels. These patterns were not consistently significant across all sites; the effects of hyperaccumulators may have been diluted by their low abundance and the relatively large area of survey. In the smaller-scale study, highly significant results were obtained, showing more bare ground, less canopy cover, and higher species richness in plots with hyperaccumulators; soil Se concentration was also higher in plots with hyperaccumulators. CONCLUSIONS: Hyperaccumulators may significantly affect local soil Se concentration and vegetation over at least a 3 m diameter area, or 4× their canopy. These differences may result from the combined positive and negative allelopathic effects observed earlier at the organismal level.

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In these studies we identified and compared the properties of plant species that showed positive or negative co-occurrence with selenium (Se) hyperaccumulators in their natural habitat. The main questions addressed were: which species are most abundant directly adjacent to hyperaccumulators, and which are absent? How do Se accumulation and tolerance compare in species found to positively or negatively co-occur with hyperaccumulators? Approaches included field surveys, X-ray microprobe analysis of field samples, and a lab Se tolerance and accumulation study. When 54 hyperaccumulators across two naturally seleniferous sites were surveyed for their five nearest neighboring species, and the relative abundance of these species around hyperaccumulators compared to that in the overall vegetation, some species were identified to positively or negatively co-occur with hyperaccumulators. Several positively co-occurring species showed high Se accumulation capability (up to 900 mg Se per kg dry weight), which may reflect Se tolerance. Leaf X-ray microprobe analysis found relatively more organic forms of Se in two positively co-occurring species than in a negatively co-occurring one. There were elevated soil Se levels around Se hyperaccumulators, and neighbors of Se hyperaccumulators had a higher tissue Se concentration as compared to when the same species grew elsewhere in the area. The elevated soil Se levels around Se hyperaccumulators - likely resulting from litter deposition- may significantly affect the local plant community, facilitating Se-tolerant plant community members but lowering the fitness of Se-sensitive members.

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BACKGROUND: The plant Stanleya pinnata hyperaccumulates Se up to 0.5% of its dry weight in organic forms, whereas the closely related Stanleya elata does not hyperaccumulate Se. ATP sulfurylase (ATPS) can catalyze the formation of adenosine 5'-phosphoselenate (APSe) from ATP and selenate. We investigated the S. pinnata ATPS2 isoform (SpATPS2) to assess its possible role in Se hyperaccumulation. METHODS: ATPS expression and activity was compared in the two Stanleya species. The ATPS2 protein sequences were modeled. Sub-cellular locations were analyzed using GFP fusions. Enzyme activity of purified recombinant SpATPS2 was measured. RESULTS: ATPS2 transcript levels were six-fold higher in roots of S. pinnata relative to S. elata. Overall root ATPS enzyme activity was two-fold elevated in S. pinnata. Cloning and sequencing of SpATPS2 and S. elata ATPS2 (SeATPS2) showed the predicted SeATPS2 to be canonical, while SpATPS2, although very similar in its core structure, has unique features, including an interrupted plastid targeting signal due to a stop codon in the 5' region of the coding sequence. Indeed GFP fusions revealed that SpATPS2 had exclusive cytosolic localization, while SeATPS2 showed dual localization in plastids and cytosol. SpATPS2 activity was inhibited by both sulfate and selenate, indicating that the enzyme acts on both substrates. CONCLUSIONS: The ATPS2 from S. pinnata differs from non-accumulator ATPS2 in its elevated expression and sub-cellular localization. It likely acts on both selente and sulfate substrates. GENERAL SIGNIFICANCE: These observations shed new light on the role of ATPS2 in the evolution of Se hyperaccumulation in plants. This article is part of a Special Issue entitled Selenium research in biochemistry and biophysics - 200 year anniversary issue, edited by Dr. Elias Arnér and Dr. Regina Brigelius-Flohe.