Effects of metal amendment and metalloid supplementation on foliar defences are plant accession-specific in the hyperaccumulator Arabidopsis halleri

Abstract

Soil pollution by metals and metalloids as a consequence of anthropogenic industrialisation exerts a seriously damaging impact on ecosystems. However, certain plant species, termed hyperaccumulators, are able to accumulate extraordinarily high concentrations of these metal(loid)s in their aboveground tissues. Such hyperaccumulation of metal(loid)s is known to act as a defence against various antagonists, such as herbivores and pathogens. We investigated the influences of metal(loid)s on potential defence traits, such as foliar elemental, organic and mechanical defences, in the hyperaccumulator plant species Arabidopsis halleri (Brassicaceae) by artificially amending the soil with common metallic pollutants, namely cadmium (Cd) and zinc (Zn). Additionally, unamended and metal-amended soils were supplemented with the metalloid silicon (Si) to study whether Si could alleviate metal excess. Individuals originating from one non-/low- and two moderately to highly metal-contaminated sites with different metal concentrations (hereafter called accessions) were grown for eight weeks in a full-factorial design under standardised conditions. There were significant interactive effects of metal amendment and Si supplementation on foliar concentrations of certain elements (Zn, Si, aluminium (Al), iron (Fe), potassium (K) and sulfur (S), but these were accession-specific. Profiles of glucosinolates, characteristic organic defences of Brassicaceae, were distinct among accessions, and the composition was affected by soil metal amendment. Moreover, plants grown on metal-amended soil contained lower concentrations of total glucosinolates in one of the accessions, which suggests a potential trade-off between inorganic defence acquisition and biosynthesis of organic defence. The density of foliar trichomes, as a proxy for the first layer of mechanical defence, was also influenced by metal amendment and/or Si supplementation in an accession-dependent manner. Our study highlights the importance of examining the effects of co-occurring metal(loid)s in soil on various foliar defence traits in different accessions of a hyperaccumulating species.

Keywords: Elemental defence; Glucosinolate; Intraspecific variation; Metal hyperaccumulation; Silicon; Trade-off hypothesis.