Plant defense resistance in natural enemies of a specialist insect herbivore

Zhang, Xi; van Doan, Cong; Arce, Carla C. M.; Hu, Lingfei; Gruenig, Sandra; Parisod, Christian; Hibbard, Bruce E.; Hervé, Maxime R.; Nielson, Chad; Robert, Christelle A. M.; Machado, Ricardo A. R.; Erb, Matthias (2019). Plant defense resistance in natural enemies of a specialist insect herbivore. Proceedings of the National Academy of Sciences of the United States of America - PNAS, 116(46), pp. 23174-23181. National Academy of Sciences NAS 10.1073/pnas.1912599116

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Plants defend themselves against herbivores through the production of toxic and deterrent metabolites. Adapted herbivores can tolerate and sometimes sequester these metabolites, allowing them to feed on defended plants and become toxic to their own enemies. Can herbivore natural enemies overcome sequestered plant defense metabolites to prey on adapted herbivores? To address this question, we studied how entomopathogenic nematodes cope with benzoxazinoid defense metabolites that are produced by grasses and sequestered by a specialist maize herbivore, the western corn rootworm. We find that nematodes from US maize fields in regions in which the western corn rootworm was present over the last 50 y are behaviorally and metabolically resistant to sequestered benzoxazinoids and more infective toward the western corn rootworm than nematodes from other parts of the world. Exposure of a benzoxazinoid-susceptible nematode strain to the western corn rootworm for 5 generations results in higher behavioral and metabolic resistance and benzoxazinoid-dependent infectivity toward the western corn rootworm. Thus, herbivores that are exposed to a plant defense sequestering herbivore can evolve both behavioral and metabolic resistance to plant defense metabolites, and these traits are associated with higher infectivity toward a defense sequestering herbivore. We conclude that plant defense metabolites that are transferred through adapted herbivores may result in the evolution of resistance in herbivore natural enemies. Our study also identifies plant defense resistance as a potential target for the improvement of biological control agents.

Item Type:

Journal Article (Original Article)

Division/Institute:

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

UniBE Contributor:

Zhang, Xi; Doan, Van Cong; Marques Arce, Carla Cristina; Hu, Lingfei; Grünig, Sandra; Parisod, Christian Gérard; Hervé, Maxime; Robert, Christelle Aurélie Maud; Machado, Ricardo and Erb, Matthias

Subjects:

500 Science > 580 Plants (Botany)

ISSN:

0027-8424

Publisher:

National Academy of Sciences NAS

Language:

English

Submitter:

Peter Alfred von Ballmoos-Haas

Date Deposited:

20 Nov 2019 15:07

Last Modified:

20 Nov 2019 15:07

Publisher DOI:

10.1073/pnas.1912599116

PubMed ID:

31659056

Uncontrolled Keywords:

tritrophic interactions; plant secondary metabolism; biological contro; lplant–herbivore interactions; coevolutionary arms race

BORIS DOI:

10.7892/boris.135368

URI:

https://boris.unibe.ch/id/eprint/135368

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