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

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

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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.

Item Type:

Journal Article (Original Article)

Division/Institute:

08 Faculty of Science > Institute of Geography
08 Faculty of Science > Department of Biology > Institute of Plant Sciences (IPS) > Biotic Interactions
08 Faculty of Science > Department of Biology > Institute of Plant Sciences (IPS)

UniBE Contributor:

Hu, Lingfei; Robert, Christelle Aurélie Maud; Züst, Tobias; Mestrot, Adrien and Erb, Matthias

Subjects:

900 History > 910 Geography & travel
500 Science > 580 Plants (Botany)

ISSN:

0027-8424

Publisher:

National Academy of Sciences NAS

Language:

English

Submitter:

Peter Alfred von Ballmoos-Haas

Date Deposited:

01 Dec 2021 11:42

Last Modified:

22 Apr 2022 03:31

Publisher DOI:

10.1073/pnas.2109602118

Related URLs:

Uncontrolled Keywords:

plant secondary metabolites; benzoxazinoids; herbivore resistance; plant herbivore interactions; maize

BORIS DOI:

10.48350/160792

URI:

https://boris.unibe.ch/id/eprint/160792

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