Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals.

Tailoring defense responses to different attackers is important for plant performance. Plants can use secondary metabolites with dual functions in resistance and defense signaling to mount herbivore-specific responses. To date, the specificity and evolution of this mechanism are unclear. Here, we studied the functional architecture, specificity, and genetic basis of defense regulation by benzoxazinoids in cereals. We document that DIMBOA-Glc induces callose as an aphid resistance factor in wheat. O-methylation of DIMBOA-Glc to HDMBOA-Glc increases plant resistance to caterpillars but reduces callose inducibility and resistance to aphids. DIMBOA-Glc induces callose in wheat and maize, but not in Arabidopsis, while the glucosinolate 4MO-I3M does the opposite. We identify a wheat O-methyltransferase (TaBX10) that is induced by caterpillar feeding and converts DIMBOA-Glc to HDMBOA-Glc in vitro. While the core pathway of benzoxazinoid biosynthesis is conserved between wheat and maize, the wheat genome does not contain close homologs of the maize DIMBOA-Glc O-methyltransferase genes, and TaBx10 is only distantly related. Thus, the functional architecture of herbivore-specific defense regulation is similar in maize and wheat, but the regulating biosynthetic genes likely evolved separately. This study shows how two different cereal species independently achieved herbivore-specific defense activation by regulating secondary metabolite production.

Plant iron acquisition strategy exploited by an insect herbivore.

Insect herbivores depend on their host plants to acquire macro- and micronutrients. Here we asked how a specialist herbivore and damaging maize pest, the western corn rootworm, finds and accesses plant-derived micronutrients. We show that the root-feeding larvae use complexes between iron and benzoxazinoid secondary metabolites to identify maize as a host, to forage within the maize root system, and to increase their growth. Maize plants use these same benzoxazinoids for protection against generalist herbivores and, as shown here, for iron uptake. We identify an iron transporter that allows the corn rootworm to benefit from complexes between iron and benzoxazinoids. Thus, foraging for an essential plant-derived complex between a micronutrient and a secondary metabolite shapes the interaction between maize and a specialist herbivore.