Lingfei Hu, Zhenwei Wu, Christelle A. M. Robert, Xiao Ouyang, Tobias Züst, Adrien Mestrot, Jianming Xu, and Matthias Erb.

PNAS October 26, 2021 118 (43) e2109602118

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.

Abstract

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.

See: https://www.pnas.org/content/118/43/e2109602118

Fig. 1.

The effect of benzoxazinoids on herbivore performance depends on the soil type. (Center) Map depicting soil collection sites around Yixing (China). Gray boxes (A–H): Growth of S. frugiperda caterpillars on WT and benzoxazinoid-deficient bx1 mutant plants growing in the different soils (+SE, n = 10), together with respective soil properties. Soil properties are depicted as fold change relative to the average across all tested soils. Refer to SI Appendix, Fig. S1 for absolute values. Soils 1 through 4 are anthrosols, and soils 5 through 8 are ferrosols. Asterisks indicate significant differences between plant genotypes (ANOVA; *P < 0.05). (I) PCA of field soil properties. Green triangles represent soils on which caterpillars grow better on WT plants. Yellow squares represent soils on which caterpillars grow better on bx1 mutant plants. Vectors of soil parameters are shown as gray arrows. (J) Iron contents in the leaves of WT and bx1 plants grown in the different soils (+SE, n = 3, with three to four individual plants pooled per replicate). For full elemental analysis, refer to SI Appendix, Fig. S4. DW, dry weight. O.C., organic carbon. Two-way ANOVA results testing for genotype and soil effects are shown (**P < 0.01; ***P < 0.001). Asterisks indicate significant differences between genotypes within the same soil (pairwise comparisons through FDR-corrected LSMeans; *P < 0.05; **P < 0.01).