Selenium transport and metabolism in plants: Phytoremediation and biofortification implications

Abstract

The aim of this review is to synthesize current knowledge of selenium (Se) transport and metabolism in plants, with a focus on implications for biofortification and phytoremediation. Selenium is a necessary human micronutrient, and around a billion people worldwide may be Se deficient. This can be ameliorated by Se biofortification of staple crops. Selenium is also a potential toxin at higher concentrations, and multiple environmental disasters over the past 50 years have been caused by Se pollution from agricultural and industrial sources. Phytoremediation by plants able to take up large amounts of Se is an important tool to combat pollution issues. Both biofortification and phytoremediation applications require a thorough understanding of how Se is taken up and metabolized by plants. Selenium uptake and translocation in plants are largely accomplished via sulfur (S) transport proteins. Current understanding of these transporters is reviewed here, and transporters that may be manipulated to improve Se uptake are discussed. Plant Se metabolism also largely follows the S metabolic pathway. This pathway is reviewed here, with special focus on genes that have been, or may be manipulated to reduce the accumulation of toxic metabolites or enhance the accumulation of nontoxic metabolites. Finally, unique aspects of Se transport and metabolism in Se hyperaccumulators are reviewed. Hyperaccumulators, which can accumulate Se at up to 1000 times higher concentrations than normal plants, present interesting specialized systems of Se transport and metabolism. Selenium hyperaccumulation mechanisms and potential applications of these mechanisms to biofortification and phytoremediation are presented.

Keywords: Glutathione; Hyperaccumulator; Selenate; Selenocysteine; Selenomethionine; Sulfate.

Graphical abstract

Fig. 1

Conceptual map of selenium transport in plants. Selenate (SeO₄²⁻) is highlighted in yellow, selenite (SeO₃²⁻) is highlighted in green, and the amino acids selenocysteine (SeCys) and selenomethionine (SeMet) are highlighted in blue. Transport of selenate via SULTR1;1 and SULTR1;2 is bolded because there is experimental evidence to support it (Barberon et al., 2008, Takahashi et al., 2000, Van Hoewyk et al., 2008). All other movement of selenocompounds is not bolded because the supporting evidence (discussed in 2.1, 2.2) is indirect and largely consists of interpretation from transcriptomic analyses. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Conceptual map of the plastidic pathway of selenium metabolism in plants. The cytosolic pathway (reduction of selenate to adenosine 5′-phosphoselenate by cytosolic ATPS) is not shown here. Plastid-localized reactions on green background; cytosol-localized reactions on blue background. All reactants are shown; for simplicity, only products containing Se are shown. Double arrows indicate steps are not shown. Compounds that are found in high concentrations in Se hyperaccumulators are bordered in bold black. Compounds that are only found in Se hyperaccumulators are bordered in bold red. Kinked double arrows indicate compounds that are volatilized. Several enzymes have alternate localizations not shown here. These include ATP sulfurylase (also found in cytosol) and cysteine synthase (also found in cytosol and mitochondria). ATP: adenosine triphosphate; OPH: O-phosphohomoserine; OAS: O-acetylserine; GSH: glutathione; MMT: S-adenosyl-L-Methionine:L-Methionine S-methyltransferase. All chemical structures obtained from PubChem database (Kim et al., 2019). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

Schema for transgenic plants with enhanced Se phytoremediation and biofortification potential. Highlighted transporters and enzymes have been experimentally manipulated in vivo; other transporters and enzymes have not. Overexpressed SULTRs are in rounded boxes. Overexpressed enzymes are italicized in dark red; selected intermediate selenocompounds are bold in black. Selenocompounds which may be highly bioaccumulated are highlighted in blue. Volatilized compounds indicated by kinked double arrows. SeO₄²⁻: selenate, SeO₃²⁻: selenite, ATPS: ATP sulfurylase, APR: APS reductase, CγS: cysteine-gamma-synthase, SMT: selenocysteine methyltransferase, SeCys: selenocysteine, MeSeCys: methylselenocysteine, SeCysTH: selenocystathionine, MMH: methylmethionine hydrolase, DMSP: dimethylsulfoniopropionate, DMSe: dimethylselenide. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)