Institute of Plant Sciences, University of Bern, Bern, Switzerland; Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
Xi Zhang
Institute of Plant Sciences, University of Bern, Bern, Switzerland
Ricardo AR Machado
Institute of Plant Sciences, University of Bern, Bern, Switzerland
Stefanie Schirmer
Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
Martina Lori
Institute of Plant Sciences, University of Bern, Bern, Switzerland
Pierre Mateo
Laboratory of Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, Neuchâtel, Switzerland
Highly adapted herbivores can phenocopy two-component systems by stabilizing, sequestering and reactivating plant toxins. However, whether these traits protect herbivores against their enemies is poorly understood. We demonstrate that the western corn rootworm Diabrotica virgifera virgifera, the most damaging maize pest on the planet, specifically accumulates the root-derived benzoxazinoid glucosides HDMBOA-Glc and MBOA-Glc. MBOA-Glc is produced by D. virgifera through stabilization of the benzoxazinoid breakdown product MBOA by N-glycosylation. The larvae can hydrolyze HDMBOA-Glc, but not MBOA-Glc, to produce toxic MBOA upon predator attack. Accumulation of benzoxazinoids renders D. virgifera highly resistant to nematodes which inject and feed on entomopathogenic symbiotic bacteria. While HDMBOA-Glc and MBOA reduce the growth and infectivity of both the nematodes and the bacteria, MBOA-Glc repels infective juvenile nematodes. Our results illustrate how herbivores combine stabilized and reactivated plant toxins to defend themselves against a deadly symbiosis between the third and the fourth trophic level enemies.
