Evolution of selenium hyperaccumulation in Stanleya (Brassicaceae) as inferred from phylogeny, physiology and X-ray microprobe analysis.

Past studies have identified herbivory as a likely selection pressure for the evolution of hyperaccumulation, but few have tested the origin(s) of hyperaccumulation in a phylogenetic context. We focused on the evolutionary history of selenium (Se) hyperaccumulation in Stanleya (Brassicaceae). Multiple accessions were collected for all Stanleya taxa and two outgroup species. We sequenced four nuclear gene regions and performed a phylogenetic analysis. Ancestral reconstruction was used to predict the states for Se-related traits in a parsimony framework. Furthermore, we tested the taxa for Se localization and speciation using X-ray microprobe analyses. True hyperaccumulation was found in three taxa within the S. pinnata/bipinnata clade. Tolerance to hyperaccumulator Se concentrations was found in several taxa across the phylogeny, including the hyperaccumulators. X-ray analysis revealed two distinct patterns of leaf Se localization across the genus: marginal and vascular. All taxa accumulated predominantly (65-96%) organic Se with the C-Se-C configuration. These results give insight into the evolution of Se hyperaccumulation in Stanleya and suggest that Se tolerance and the capacity to produce organic Se are likely prerequisites for Se hyperaccumulation in Stanleya.

Characterization of selenium and sulfur accumulation across the genus Stanleya (Brassicaceae): A field survey and common-garden experiment.

UNLABELLED: • PREMISE OF STUDY: Selenium (Se) hyperaccumulation, the capacity to concentrate the toxic element Se above 1000 mg·kg(-1)·dry mass, is found in relatively few taxa native to seleniferous soils. While Se hyperaccumulation has been shown to likely be an adaptation that protects plants from herbivory, its evolutionary history remains unstudied. Stanleya (Brassicaceae) is a small genus comprising seven species endemic to the western United States. Stanleya pinnata is a hyperaccumulator of selenium (Se). In this study we investigated to what extent other Stanleya taxa accumulate Se both in the field and a greenhouse setting on seleniferous soil.• METHODS: We collected multiple populations of six of the seven species and all four varieties of S. pinnata We tested leaves, fruit, and soil for in situ Se and sulfur (S) concentrations. The seeds collected in the field were used for a common garden study in a greenhouse.• KEY RESULTS: We found that S. pinnata var. pinnata is the only hyperaccumulator of Se. Within S. pinnata var. pinnata, we found a geographic pattern related to Se hyperaccumulation where the highest accumulating populations are found on the eastern side of the continental divide. We also found differences in genome size within the S. pinnata species complex.• CONCLUSIONS: The S. pinnata species complex has a range of physiological properties making it an attractive system to study the evolution of Se hyperaccumulation. Beyond the basic scientific value of understanding the evolution of this fascinating trait, we can potentially use S. pinnata or its genes for environmental cleanup and/or nutrient-enhanced dietary material.