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Abstract:
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.
