Extending the elemental defence hypothesis in the light of plant chemodiversity

Abstract

Summary Some plant species tolerate and accumulate high levels of metals or metalloids in their tissues. The elemental defence hypothesis posits that metal(loid) hyperaccumulation by these plants can serve as protection against antagonists. Numerous studies support this hypothesis. In addition, as other plant species, hyperaccumulators synthesise specialised metabolites that can act as organic defences. In principle, the composition and concentration of plant‐specialised metabolites vary pronouncedly not only among species, but also within species and within individuals. This variation is called chemodiversity. Surprisingly, the role of chemodiversity has received little attention in elemental defence. Thus, we advocate that the concept of the elemental defence hypothesis should be extended and linked to the multifunctionality of plant chemodiversity to better understand the eco‐evolutionary dynamics and maintenance of metal(loid) hyperaccumulation. Comprehensive literature studies revealed that both metal(loid)s and specialised metabolites acting as defences are highly diverse in some hyperaccumulators and the biosynthetic pathways of these two types of defences are partly intertwined. Several edaphic‐, population‐, temporal‐ and spatial‐related factors were found to influence metal(loid) diversity, which should be considered in the elemental defence hypothesis. We thus present a novel synthesis and outlook to extend the elemental defence hypothesis in the light of chemodiversity.

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

“…We did not find significant effects of Si supplementation on the foliar concentrations of Cd and Zn, at least in the old leaves studied here, although Si concentrations increased by 7.5% in +Si-supplemented soil relative to −Si at the end of the experiment. It is still poorly understood how and to what extent Si influences the uptake and accumulation of metals, including Cd and Zn, in metal(loid) hyperaccumulator plants (Putra and Müller 2023 ). However, in the As hyperaccumulator I. cappadocica , supplementation with Si led to a significant reduction of shoot and root concentrations of As and Cd (Azam et al 2021 ).…”

“…First, the analysis of costs and benefits between the two types of defences is difficult and should involve physiological, ecological and evolutionary assessments (Boyd 2013 ). Second, just like other plants, hyperaccumulators synthesise a plethora of specialised metabolites, and their composition and concentration may differ within species and even within an individual, termed chemodiversity (Moore et al 2014 ; Müller and Junker 2022 ), which is still overlooked in many hyperaccumulators (Putra and Müller 2023 ). Third, trade-offs may be more relevant in the context of induced resistance (Fones and Preston 2013 ; Tewes et al 2018 ; Fones et al 2019 ).…”

“…Such plants may be used to remediate metal(loid)-contaminated sites and mitigate the far-reaching adverse consequences of soil pollutant metal(loid)s for the environment (Rylott and Bruce 2022 ). Fundamental studies on the combined effects of different metal(loid)s, which often co-occur in soils, on hyperaccumulators are still lacking (Putra and Müller 2023 ). Moreover, responses to co-occurring metal(loid)s may differ between populations within the same species.…”

“…Likewise, high Si accumulation in the foliage and in trichomes resulted in a potent mechanical defence in O. sativa against folivores (Andama et al 2020 ). In addition to elemental and mechanical defences acquired through metal(loid) hyperaccumulation, hyperaccumulators also contain numerous specialised metabolites that can act as organic defences against antagonists (Putra and Müller 2023 ). The biosynthesis of specialised metabolites is considered to be more costly than metal(loid) hyperaccumulation (Boyd 2013 ).…”

Changes in the Biology and Susceptibility of Weevil (Cylas formicarius) to the Insecticide Spinetoram as a Response to Cadmium Contamination

“…The effects of heavy metals have been examined in a variety of plants (e.g., rice, maize, soybean, kale), as well as in coleopteran, hemipteran, dipteran, lepidopteran, and orthopteran insects [ 3 , 6 , 15 , 16 , 17 , 18 , 19 , 20 ]. Among hypotheses to explain metal hyperaccumulation in plants, the elemental defense hypothesis is the most widely tested, and it proposes that metals accumulate in plant tissues to defend against insect herbivory [ 3 , 21 , 22 , 23 , 24 ]. Esteves-Aguilar et al [ 25 ] reported that heavy metal exposure increases physical and chemical defenses against herbivores in Wigandia urens Kunth (Boraginaceae), a shrub or small tree.…”