Exploring plant defenses against herbivory in the Brassicaceae: Tradeoff or joint defense?
Plants in the Brassicaceae have evolved a variety of defenses against herbivores, including chemical defenses (glucosinolates), physical defenses (trichomes), and elemental defenses (accumulating toxic elements). For species that accumulate toxic metals, the “trade-off hypothesis” predicts that investment in constitutive organic defenses may decrease (Davis and Boyd, 2000). The relationship between elemental and organic defenses is complex however, and the “joint-effects hypothesis” predicts that both kinds of defenses may act together against herbivores (Maestri et al. 2010, Boyd 2012). This study addressed the following questions: (1) do leaf glucosinolate concentrations differ when plants occur in soil environments with and without Ni? and, (2) does glucosinolate production differ between closely-related Ni-accumulator and non-accumulator species in the Brassicaceae? Three sets of congeneric species were selected, contrasting a Ni-hyperaccumulator and a non-accumulator. The hyperaccumulators were Alyssum murale, Alyssum corsicum, Streptanthus polygaloides, and Noccea fendleri. The non-accumulators were Alyssum montanum, Streptanthus brewerii, and Thlaspi arvense. Plants were grown in a lath house at UC Davis in summer 2014 using two soil treatments: High Ni (500 ppm Ni added) and Low Ni (0 ppm added). Glucosinolates were measured by HPLC, and Ni uptake was measured by inductively coupled plasma atomic absorption spectroscopy (Broadhurst et al. 2004).
Leaf glucosinolate values were analyzed for the effects of accumulator status (with species nested as a random effect), the effect of soil environment (High vs Low Ni), as well as the interaction between these factors. Shoot biomass was included as covariate. Soil nickel concentration had a significant effect on glucosinolate production, and the interaction between accumulator status and soil environment was significant. For hyperaccumulator species, both total glucosinolates and glucosinolate richness decreased in soil with Ni. This pattern was not seen in non- accumulator species. Aliphatic glucosinolates predominated, with smaller quantities of indolic and branched chain glucosinolates. In both soil environments, the three species in the genus Alyssum produce lower glucosinolate levels than other species examined. In A. murale and A. corsicum, leaves contained 14,700 -20,500 ppm Ni, and shoot biomass was greater in the High Ni treatment. Overall, these results support the trade-off hypothesis since a lower level of organic defense was found in hyperaccumulators that occupy a soil environment providing access to toxic soil elements for defense. Hyperaccumulator species in the Brassicaceae may switch from chemical defense to elemental defense in a context-dependent fashion.