The role of selenium in protecting plants against prairie dog herbivory: implications for the evolution of selenium hyperaccumulation

Abstract

Some plants can hyperaccumulate the element selenium (Se) up to 10,000 mg Se kg(-1) dry weight. Hyperaccumulation has been hypothesized to defend against herbivory. In laboratory studies high Se levels protect plants from invertebrate herbivores and pathogens. However, field studies and mammalian herbivore studies that link Se accumulation to herbivory protection are lacking. In this study a combination of field surveys and manipulative field studies were carried out to determine whether plant Se accumulation in the field deters herbivory by black-tailed prairie dogs (Cynomys ludovicianus). The Se hyperaccumulator Astragalus bisulcatus (two-grooved milkvetch) occurs naturally on seleniferous soils in the Western USA, often on prairie dog colonies. Field surveys have shown that this Se hyperaccumulator is relatively abundant on some prairie dog colonies and suffers less herbivory than other forb species. This protection was likely owing to Se accumulation, as judged from subsequent manipulative field experiments. When given a choice between pairs of plants of the Se hyperaccumulator Stanleya pinnata (prince's plume) that were pretreated with or without Se, prairie dogs preferred to feed on the plants with low Se; the same results were obtained for the non-hyperaccumulator Brassica juncea (Indian mustard). Plants containing as little as 38 mg Se kg(-1) DW were protected from herbivory. Taken together these results shed light on the functional significance of Se hyperaccumulation and the possible selection pressures driving its evolution. They also have implications for the use of plants in Se phytoremediation, or as Se-fortified crops.

Water relations of yellow sweetclover under the synergy of drought and selenium addition

“…Many hypotheses have been proposed to explain the functional significance of metal and metalloid hyperaccumulation by plants, including allelopathy (Boyd and Martens 1998), protection from herbivores and pathogens (Davis et al 2001;Quinn et al 2008) and drought resistance (Boyd and Martens 1998). According to the last hypothesis metal hyperaccumulation is assumed to improve plant resistance to water deficit by reducing either transpirational losses or osmotic potential.…”

Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata

“…The hyperaccumulators Astragalus bisulcatus and Stanleya pinnata were found to predominantly accumulate Se in peripheral tissues of young leaves and reproductive organs: in structures important to protect, prone to herbivore and pathogen attacks, and/or typically associated with playing a defensive role (Pickering et al, 2003a;Freeman et al, 2006b;Galeas et al, 2007). Indeed, laboratory and field studies have shown that Se can protect plants from various herbivores and fungal pathogens (Vickerman and Trumble, 1999;Bañ uelos et al, 2002;Hanson et al, 2003Hanson et al, , 2004Freeman et al, 2006aFreeman et al, , 2007Freeman et al, , 2009Galeas et al, 2008;Quinn et al, 2008).…”

Evolutionary aspects of elemental hyperaccumulation

“…Zinc and Cd can Table 1 also protect plants from invertebrate herbivory (Pollard and Bakers 1997;Jhee et al 1999). Similarly, Se can protect plants from a variety of herbivores and pathogens, including moth and butterfly larvae, aphids, thrips, spider mites, grasshoppers, prairie dogs, as well as fungal pathogens (vickerman and Trumble 1999;Hanson et al 2004;Freeman et al 2006bFreeman et al , 2007Freeman et al , 2009Quinn et al 2008Quinn et al , 2010a. Arsenic has also been shown to protect plants from herbivores (Mathews et al 2009).…”