Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 118, Issue 43, Pages -Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2109602118
Keywords
plant secondary metabolites; benzoxazinoids; herbivore resistance; plant herbivore interactions; maize
Categories
Funding
- National Natural Science Foundation of China [41721001, 42007029, 42090061]
- Young Elite Scientists Sponsorship Program by the China Association for Science and Technology [2020QNRC002]
- Interfaculty Research Collaboration One Health of the University of Bern
- Fundamental Research Funds for the Central Universities [2020QNA6009]
- Schweizerischer Nationalfonds zur Forderung der Wissenschaftlichen Forschung [310030_189071]
- Swiss National Science Foundation (SNF) [310030_189071] Funding Source: Swiss National Science Foundation (SNF)
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Plant secondary metabolites play a dual role in plant defense and root interactions with herbivores, with soil iron levels influencing the impact of these metabolites on herbivore growth. This study highlights the complex interplay between soil chemistry and plant defense mechanisms, demonstrating the multifunctionality of plant secondary metabolites in shaping interactions in variable environments.
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.
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