Nickel hyperaccumulation by Streptanthus polygaloides is associated with herbivory tolerance

Abstract

Metal hyperaccumulation can increase plant resistance to herbivory, but tolerance as an herbivore defense has been little investigated. This study explored the interaction between Ni hyperaccumulation and herbivory tolerance using Streptanthus polygaloides. Plants were grown in one of two potting soil Ni treatments: Ni‐amended (800 µg g−1 added Ni) or unamended (0 µg g−1 added Ni). One‐month‐old plants were arbitrarily assigned one of four levels of artificial herbivory damage applied to the leaves. Response variables included aboveground dry biomass and Ni concentration, total leaf number, final plant height, and total number of flowers, and were analyzed by two‐way ANOVA. We found no consistent soil Ni effect, artificial herbivory effect, or interaction between soil Ni and artificial herbivory treatments for total leaf number or final plant height. However, there was a soil Ni effect for biomass, flower production, and Ni concentrations: all were greater for plants grown in Ni‐amended soil when compared to plants grown in unamended soil. There was also a significant interaction between treatments for number of flowers produced (reflecting plant fitness) as well as for aboveground biomass. Plants of S. polygaloides receiving greater damage produced significantly more flowers, and had greater biomass, when grown in Ni‐amended soil than plants in unamended soil. We conclude that Ni hyperaccumulation is associated with herbivory tolerance of S. polygaloides, increasing plant fitness when herbivory damage is severe. Herbivory tolerance provides an additional dimension to elemental defenses that can supplement the defense trait of herbivory resistance.

Nickelophilic root foraging by the nickel hyperaccumulator, Streptanthus polygaloides subsp. undulatus (Brassicaceae)

“…Kazemi‐Dinan et al (2015) performed a common garden experiment that supports the idea that Cd and Zn hyperaccumulation can reduce herbivore attack and improve the performance of Arabidopsis halleri (L.) O'Kane and Al‐Shehbaz. Several other studies (Ghasemi et al, 2014; Isnard et al, 2020; Meindl & Ashman, 2017; Mincey et al, 2018) also suggest that a hyperaccumulated element improves growth or reproductive potential of a hyperaccumulator. Our study's results are in accord with the “elemental stimulation” hypothesis, as Ni enhanced root growth and stimulated lateral root production occurred in S. polygaloides .…”

“…It is the only species of the genus that hyperaccumulates Ni (Kruckeberg & Reeves, 1995; Reeves et al, 1981). It is also the most‐investigated North American Ni hyperaccumulator, as it has been the subject of studies of morphology, ecology, genetics, herbivore interactions, and elemental concentration (e.g., Boyd et al, 2000, 2009; Davis et al, 2001; Jhee et al, 2006; Mincey et al, 2018; Mincey & Boyd, 2018; Pope et al, 2013). Streptanthus insignis Jeps.…”

Recent advances in the study of serpentine plants and ecosystems: Perspectives from the 10th International Conference on Serpentine Ecology, France

“…Inoue et al (2024) studied a rare species ( Saussurea ochiaiana ) from Japan and showed that habitat conditions suitable for the regeneration of this species are decreasing because of climate change and the depopulation of rural communities, implying that urgent conservation strategies are needed. Mincey and Boyd (2024) report on root foraging by the Ni hyperaccumulator Streptanthus polygaloides from the United States and found that it exhibited positive root foraging responses which they termed “nickelophilic root foraging.” Their findings suggest that Ni hyperaccumulation has adaptive value, as opposed to the nonadaptive “inadvertent uptake” hypothesis that was listed by Boyd and Martens (1992) as a potential explanation for hyperaccumulation in a seminal paper published in the proceedings of the 1st ICSE (held in Davis, California, USA) and updated by Boyd (2014). Sherri et al (2024) investigated the effect of polycyclic aromatic hydrocarbons and trace elements on antioxidant response and phytoextraction efficiency in Noccaea caerulescens .…”