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

Abstract

SummaryPast 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.

Transcriptome‐wide comparison of selenium hyperaccumulator and nonaccumulator Stanleya species provides new insight into key processes mediating the hyperaccumulation syndrome

“…The difference between cgs and cbl transcript levels was even higher in S. elata, which may indicate that S. elata accumulates a larger fraction of its organic Se as selenocystathionine. Cappa et al (2015) found 75% organic Se in S. elata, which is similar to that in nonhyperaccumulator S. albescens, whose organic Se fraction was found to consist of exclusively selenocystathionine (Freeman et al, 2010); the same may be the case for S. elata.…”

“…Cappa et al . () found 75% organic Se in S. elata , which is similar to that in nonhyperaccumulator S. albescens , whose organic Se fraction was found to consist of exclusively selenocystathionine (Freeman et al ., ); the same may be the case for S. elata .…”

“…The higher transcript levels of S/Se assimilation genes in S. pinnata are in agreement with earlier findings from a ~350‐gene macroarray study (Freeman et al ., ) and explain the finding that S. pinnata accumulated no detectable inorganic Se, whereas S. elata contained 20%–25% inorganic Se (Cappa et al ., ). More efficient conversion from inorganic to organic Se likely is one of the Se hypertolerance mechanisms in S. pinnata .…”

“…To obtain insight into Se hyperaccumulation and hypertolerance mechanisms in S. pinnata, we investigated transcriptomewide differences in gene expression between S. pinnata and the Se nonaccumulator Stanleya elata (El Mehdawi et al, 2012). Phylogenetic and physiological analyses of the Stanleya genus showed S. elata to be one of four species in a clade that is sister to S. pinnata and Se hyperaccumulation to be an apomorphy in the S. pinnata species complex (Cappa et al, 2015). The two selected species were grown in the presence or absence of selenate and compared with respect to growth, Se and S accumulation and their root and shoot transcriptomes via RNA sequencing.…”

Variation in the angiosperm ionome

“…Congo), where natural Cu/Co outcrops occur, and many of these species have been shown to hyperaccumulate both Cu and Co (Lange et al ). The multiple incidences of the evolution of Se hyperaccumulation among eudicots (Cappa and Pilon‐Smits , White ), and in species within the Astragalus [Fabaceae] (White ) and Stanleya [Brassicaceae] (Cappa et al ) genera, have led to an explanation of the evolution of this trait, from the acquisition of tissue Se‐tolerance and the colonisation of an environmental niche to the benefits of Se‐hyperaccumulation in defence against herbivores, alleviation of oxidative stress and allelopathy (El Mehdawi and Pilon‐Smits , Schiavon and Pilon‐Smits ).…”