Metals or metabolites? Leafy volatile metabolomics revealed a trade-off between elemental defense and organic defense in Zn/Cd hyperaccumulator Sedum alfredii

Understanding the defensive strategies of hyperaccumulators in plant-herbivore interactions is essential for their safe applications in phytoremediation. Sedum alfredii plants are widely applied in metal-contaminated soil where they were found to be easily damaged by herbivores. Thus, we investigated a comparative analysis of the defensive strategies from the perspective of constitutive leafy volatiles between the hyperaccumulator S. alfredii plant and its non-hyperaccumulator counterpart, along with feeding preference tests. Generalist snails prefer hyperaccumulators with lower content of metals while detested non-hyperaccumulators with relatively high food qualities in saccharides. Further leafy volatile profiles of the two ecotypes showed a total of 34 differentially enriched metabolites with 16 down-regulated organic compounds in the hyperaccumulators. KEGG pathway enrichment analysis showed two down-regulated metabolic pathways in phenylalanine metabolism and metabolic pathways due to the lower production of naphthalene and benzeneacetaldehyde, which are known herbivore deterrents and predator attractants. Hence, the high reliance on metals with the reduced performance of organic defense implied a trade-off between the two defensive strategies in the hyperaccumulator S. alfredii plants. Overall, this increased susceptibility to herbivores due to the lack of metals advocates the concerns and solutions for the safe application of this species in the phytoremediation practice.