Restoring (E)-β-Caryophyllene Production in a Non-producing Maize Line Compromises its Resistance against the Fungus Colletotrichum graminicola

The sesquiterpene (E)-beta-caryophyllene is emitted from maize (Zea mays) leaves and roots in response to herbivore attack. This compound serves as a signal for the attraction of herbivore enemies and is present in most European maize varieties. However, most North American maize lines have lost the ability to produce (E)-beta-caryophyllene. Previously, we showed that restoring the ability to synthesize (E)-beta-caryophyllene in a non-producing maize line improved its resistance against the root herbivore Diabrotica virgifera virgifera. However, it is largely unknown whether this modification affects the resistance to other pests. In this study, we investigated the response of constitutively (E)-beta-caryophyllene-producing transgenic lines to infection by a hemibiotrophic fungus Colletotrichum graminicola. Our results showed that restoring (E)-beta-caryophyllene synthesis in a Hi-II genetic background enhanced the susceptibility of the plant to C. graminicola infection rather than increasing its resistance. This modification did not alter the baseline levels of plant defense hormones and metabolites. Nor did (E)-beta-caryophyllene production modify the expression of anti-fungal defense genes. Instead, the addition of (E)-beta-caryophyllene seemed to directly stimulate fungal growth. In an in vitro antifungal assay, we found that (E)-beta-caryophyllene stimulated hyphal growth of C. graminicola and Fusarium graminearum. Thus, although restoring (E)-beta-caryophyllene production in a non-producing maize line may improve the resistance of the plant against herbivores, it may compromise its resistance to major fungal pathogens. This might explain the loss of (E)-beta-caryophyllene during maize breeding in environments where C. graminicola and Fusarium graminearum are prevalent.