Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth

Autor: Jianming Xu, Xiao Ouyang, Matthias Erb, Zhenwei Wu, Lingfei Hu, Adrien Mestrot, Tobias Züst, Christelle A. M. Robert
Rok vydání: 2021
Předmět:
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Hu, Lingfei; Wu, Zhenwei; Robert, Christelle A. M.; Ouyang, Xiao; Züst, Tobias; Mestrot, Adrien; Xu, Jianming; Erb, Matthias (2021). Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth. Proceedings of the National Academy of Sciences of the United States of America-PNAS, 118(43), e2109602118. National Academy of Sciences NAS 10.1073/pnas.2109602118
ISSN: 1091-6490
Popis: Significance This study demonstrates that the protective effects of multifunctional maize secondary metabolites against a major pest are dependent on soil chemical composition. By functioning as both digestibility reducers and siderophores, benzoxazinoids link soil chemistry to plant–environment interactions. Given that many plant secondary metabolites have multiple functions in roots and leaves, such links are likely widespread and may govern community composition and pest dynamics across different (agro)ecosystems. The presented findings also illustrate the limits and context dependency of using multifunctional plant secondary metabolites to combat major herbivore pests. The latter is particularly important in the context of the threat that the fall armyworm poses for global maize production.
Plant secondary (or specialized) metabolites mediate important interactions in both the rhizosphere and the phyllosphere. If and how such compartmentalized functions interact to determine plant–environment interactions is not well understood. Here, we investigated how the dual role of maize benzoxazinoids as leaf defenses and root siderophores shapes the interaction between maize and a major global insect pest, the fall armyworm. We find that benzoxazinoids suppress fall armyworm growth when plants are grown in soils with very low available iron but enhance growth in soils with higher available iron. Manipulation experiments confirm that benzoxazinoids suppress herbivore growth under iron-deficient conditions and in the presence of chelated iron but enhance herbivore growth in the presence of free iron in the growth medium. This reversal of the protective effect of benzoxazinoids is not associated with major changes in plant primary metabolism. Plant defense activation is modulated by the interplay between soil iron and benzoxazinoids but does not explain fall armyworm performance. Instead, increased iron supply to the fall armyworm by benzoxazinoids in the presence of free iron enhances larval performance. This work identifies soil chemistry as a decisive factor for the impact of plant secondary metabolites on herbivore growth. It also demonstrates how the multifunctionality of plant secondary metabolites drives interactions between abiotic and biotic factors, with potential consequences for plant resistance in variable environments.
Databáze: OpenAIRE