Complex plant metabolomes guide fitness-relevant foraging decisions of a specialist herbivore

Abstract

Plants produce complex mixtures of primary and secondary metabolites. Herbivores use these metabolites as behavioral cues to increase their fitness. However, how herbivores integrate primary and secondary metabolites into fitness-relevant foraging decisions in planta is poorly understood. We developed a molecular manipulative approach to modulate the availability of sugars and benzoxazinoid secondary metabolites as foraging cues for a specialist maize herbivore, the western corn rootworm. By disrupting benzoxazinoid biosynthesis in maize and sugar perception in the western corn rootworm, we show that sugars and benzoxazinoids act as distinct and dynamically integrated mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish post-embryonic from less nutritious embryonic roots, benzoxazinoids are specifically required for the latter. Host acceptance in the form of root damage is increased by benzoxazinoids and sugars in an additive manner. This pattern is driven by increasing damage to post-embryonic roots in the presence of benzoxazinoids and sugars. Benzoxazinoid- and sugar-mediated foraging directly improves western corn rootworm growth and survival. Interestingly, western corn rootworm larvae retain a substantial fraction of their capacity to feed and survive on maize plants in the absence of both cues. This study unravels fine-grained differentiation and integration of primary and secondary metabolites into herbivore foraging and documents how the capacity to compensate for the absence of important chemical cues enables a specialist herbivore to survive within unpredictable metabolic landscapes.

In a belowground multitrophic interaction, Trichoderma harzianum induces maize root herbivore tolerance against Phyllophaga vetula

“…In this work, we found that T. harzianum triggered the release of the root terpenes α‐cubebene and (±)‐camphor and induced the emission de novo of β‐caryophyllene with respect to control plants. A similar response in the emission of volatile sesquiterpenes was identified in maize roots attacked by D. virgifera virgifera .3 Herbivore arthropods use chemosensory receptors to perceive plant‐derived chemical signals and to locate suitable plants and avoid unsuitable plants as hosts 37,40 . In particular, D. virgifera virgifera behaves according to different chemical signals that include CO 2 , aromatic organic compounds and volatile terpenes 37 .…”

“…Glucose and sucrose as components of plant sugar blends have been shown to stimulate insect feeding 5 . In fact, the western corn rootworm ( Diabrotica virgifera virgifera ) prefers to feed on roots with a higher carbohydrate content 37 . As products derived from photosynthesis, carbohydrates are the principal source of stored energy for both plants and herbivorous arthropods 5 .…”

Virus‐induced plant volatiles mediate the olfactory behaviour of its insect vectors

“…All data were analysed using SPSS 20.0 software. GRLHs feeding preference data were analysed by Wilcoxon's signed-ranks tests (Hu et al, 2020;Machado et al, 2020). A non-parametric test (Friedman-ANOVA, p < .05) for dependent data on olfactory behaviour assays of GRLHs, including plant odour preference and individual compounds was used, and differences attributed to fields using Wilcoxon-Wilcox as a post-hoc test (Faucher, Forstreuter, Hilker, & de Bruyne, 2006).…”

Western Corn Rootworm, Plant and Microbe Interactions: A Review and Prospects for New Management Tools

“…Interestingly, the application of the Fe(III)(DIMBOA) 3 complex on rice or barley, two non-host plant species for the WCR, was sufficient to trigger WCR feeding [ 41 ]. Experiments with benzoxazinoid-deficient plants and WCR larvae with impaired capacities to detect sugars confirmed the importance of the individual and combined cues for WCR foraging, but also revealed considerable WCR robustness to disruption of individual cues [ 42 ]. This may complicate attempts to use single cues for foraging disruption.…”