The plant metabolome guides 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 combine and integrate different metabolite classes 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 sugar perception in the western corn rootworm and benzoxazinoid production in maize, we show that sugars and benzoxazinoids act as distinct and dynamically combined mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish postembryonic 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 postembryonic 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 even when both classes of chemical cues are almost completely absent. This study unravels fine-grained differentiation and combination of primary and secondary metabolites into herbivore foraging and documents how the capacity to compensate for the lack of important chemical cues enables a specialist herbivore to survive within unpredictable metabolic landscapes.

Pseudocitrobacter anthropi reduces heavy metal uptake and improves phytohormones and antioxidant system in Glycine max L.

“…On the other hand, in C18 associated seedlings, higher avonoid accumulation was recorded in the host tissue and lower quantities were exuded in the rhizosphere (Machado et al 2021). This is possibly due to the reason that the avonoids act as nonenzymatic antioxidant and metal quencher.…”

Integrated view of plant metabolic defense with particular focus on chewing herbivores

“…Time‐of‐flight (TOF)‐MS has been instrumental in discovery of novel defense metabolites but it often provides too many mass features in plant extracts that, even though affected by herbivory, cannot be identified. For instance, hundreds of regulated ions (and thus potential defense compounds) have been reported in cabbage (Jansen et al, 2009), tobacco (Gulati et al, 2013; Li et al, 2015), oak (Kersten et al, 2013), maize (Marti et al, 2013; Machado et al, 2021), rice (Alamgir et al, 2016) and black mustard (Ponzio et al, 2017; Papazian et al, 2019), but only a fraction of them has actually been resolved to the structural level (Maag et al, 2015). Even closely related species of plants can show differential metabolic responses to identical herbivores (Riach et al, 2015), which further emphasizes the enormous complexity and scale of specialized metabolism in plants.…”

A beta-glucosidase of an insect herbivore determines both toxicity and deterrence of a dandelion defense metabolite

“…First, the recognition of TA-G through deglucosylation may guide the M. melolontha larva to feeding sites that are most suitable for fast larval growth, independently of the toxicity of TA-G. Exploitation of plant secondary metabolites and sugars to locate nutritious tissue has been reported, for instance, for the specialist root herbivore Diabrotica virgifera virgifera feeding on maize roots ( Robert et al, 2012 ; Hu et al, 2018 ; Machado et al, 2021 ). Melolontha melolontha larvae preferentially feed on side roots of dandelions, which contain lower TA-G and higher soluble protein levels than main roots and also may be more nutritious as they are actively growing ( Huber et al, 2016b ).…”