Testing optimal defense theory: Root resistance selection in chicory (Cichorium intybus) reduces foliar defense and alters aphid performance and feeding behavior.

BACKGROUND: Plants are constantly exposed to a wide range of herbivores at both aboveground (AG) and belowground (BG) levels, involving multiple constitutive defenses in leaves and roots. However, the Optimal Defense Theory predicts that the energy cost of defenses prevents plants from defending all organs equally. In an agroeconomic context, selecting genotypes for their root-specific resistance may therefore create trade-offs in the allocation of constitutive defenses, potentially leaving leaves more vulnerable to aerial herbivores. To test this hypothesis, we assessed the resistance to the root-feeding aphid Pemphigus bursarius (BG) and the foliar aphids Myzus persicae and Nasonovia ribisnigri (AG) in two chicory (Cichorium intybus var foliosum) genotypes: AX, considered susceptible, and B18, considered resistant to P. bursarius. Aphids' survival and fecundity were measured, and their feeding behavior was evaluated using the electrical penetration graph (EPG) technique. RESULTS: Only the root-feeding aphid P. bursarius exhibited reduced survival, fecundity and feeding activity on the B18 genotype, compared with the susceptible AX genotype, confirming the root-level resistance for which this line was originally selected. In contrast, the foliar aphid N. ribisnigri showed enhanced feeding activity and fecundity on B18, whereas M. persicae displayed only increased feeding activity, suggesting increased foliar susceptibility relative to AX. CONCLUSION: Selection for root resistance may promote a shift in resource allocation toward root defenses, potentially reducing constitutive defenses in leaves. These results highlight potential trade-offs in plant defense allocation and underline the importance of considering multi-organ herbivory when breeding for resistance traits.