Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata

Abstract

The molecular mechanisms responsible for selenium (Se) tolerance and hyperaccumulation were studied in the Se hyperaccumulator Stanleya pinnata (Brassicaceae) by comparing it with the related secondary Se accumulator Stanleya albescens using a combination of physiological, structural, genomic, and biochemical approaches. S. pinnata accumulated 3.6-fold more Se and was tolerant to 20 mM selenate, while S. albescens suffered reduced growth, chlorosis and necrosis, impaired photosynthesis, and high levels of reactive oxygen species. Levels of ascorbic acid, glutathione, total sulfur, and nonprotein thiols were higher in S. pinnata, suggesting that Se tolerance may in part be due to increased antioxidants and up-regulated sulfur assimilation. S. pinnata had higher selenocysteine methyltransferase protein levels and, judged from liquid chromatography-mass spectrometry, mainly accumulated the free amino acid methylselenocysteine, while S. albescens accumulated mainly the free amino acid selenocystathionine. S. albescens leaf x-ray absorption near-edge structure scans mainly detected a carbon-Se-carbon compound (presumably selenocystathionine) in addition to some selenocysteine and selenate. Thus, S. albescens may accumulate more toxic forms of Se in its leaves than S. pinnata. The species also showed different leaf Se sequestration patterns: while S. albescens showed a diffuse pattern, S. pinnata sequestered Se in localized epidermal cell clusters along leaf margins and tips, concentrated inside of epidermal cells. Transcript analyses of S. pinnata showed a constitutively higher expression of genes involved in sulfur assimilation, antioxidant activities, defense, and response to (methyl)jasmonic acid, salicylic acid, or ethylene. The levels of some of these hormones were constitutively elevated in S. pinnata compared with S. albescens, and leaf Se accumulation was slightly enhanced in both species when these hormones were supplied. Thus, defense-related phytohormones may play an important signaling role in the Se hyperaccumulation of S. pinnata, perhaps by constitutively up-regulating sulfur/Se assimilation followed by methylation of selenocysteine and the targeted sequestration of methylselenocysteine.

Sodium selenite treatment of vegetable seeds and seedlings and the effect on antioxidant status

“…1). In Stanleya pinnata, a selenium hyperaccumulator plant, Freeman et al (2010) found that the presence of Se in the form of Se 6+ induced higher vitamin C contents, possibly as a response to oxidative stress caused by the high concentration of Se.…”

“…The ability to donate electrons to the system is higher when the ORP value is lower. The increase in electron delivery may be related to increased activity of antioxidant enzymes, which was found in the presence of specific Se concentrations (Freeman et al, 2010).…”

Evolutionary aspects of elemental hyperaccumulation

“…at levels comparable to those in non-hyperaccumulator plants present under S starvation (Cabannes et al 2011). Similarly, several genes encoding sulfate transporters are constitutively upregulated in the Se hyperaccumulator S. pinnata relative to the non-hyperaccumulator S. albescens (Freeman et al 2010). Thus, constitutive expression of sulfate transporters may be one of the mechanisms of Se hyperaccumulation.…”

“…Glutathione (GSH) may contribute to tolerance not only by binding toxic elements, but also by scavenging free radicals. Levels of GSH were found to be constitutively enhanced in Ni hyperaccumulator Noccaea goesingense (Freeman et al 2004), as well as in Se hyperaccumulator Stanleya pinnata (Freeman et al 2010). In Phytolacca americana, a Cd hyperaccumulator, the tissue concentration of GSH was shown to increase when supplied with Cd (Zhao et al 2011).…”

“…Plants can also form volatile dimethylselenide (DMSe) from SeMet (Terry et al 2000). A transcriptome study showed that in the hyperaccumulator Stanleya pinnata many genes from the S assimilation pathway were upregulated, as compared to non-hyperaccumulator S. albescens, perhaps due to higher levels of the plant-growth regulators, jasmonate, salicylate and ethylene (Freeman et al 2010). This may explain the hyperaccumulator's higher levels of Se and S. The forms of Se in hyperaccumulators and non-hyperaccumulators are also different: while many non-hyperaccumulators accumulate predominantly selenate when treated with selenate, hyperaccumulators tend to accumulate organic Se.…”