Optimal chemical defence allocation in roots: where, why and how?

Abstract

AbstractPlants produce a range of volatile and non-volatile plant secondary metabolites (PSMs) to increase their resistance to biotic threats. The optimal defence allocation theory (ODT) states that the most valuable and vulnerable plant organs should be best defended against herbivory and therefore contain high concentrations of PSMs. However, the production of PSMs can come with metabolic and ecological costs and should be adjusted to the predictability and nature of biotic interactions to minimise interference with the ecological functions of the tissue. The ODT has recently been extended to explain PSM allocation patterns over root organs. Recent research has revealed that valuable but vulnerable root classes, such as taproots or adventitious roots, indeed have higher levels of anti-herbivory PSMs than lateral or fine roots. In this perspective, we analyse how interactions with soil organisms, including insect herbivores and microorganisms, may shape PSM allocation patterns in roots. We thereby focus on the Brassicaceae family and the glucosinolate-myrosinase defence system, but also highlight relevant studies in other species. We summarise the state-of-the-art knowledge of GSL distribution patterns over the plant body, discuss potential drivers of PSM allocation and discuss which mechanisms might regulate constitutive and induced PSM allocation patterns. Finally, we argue that implementing microbial interactions into ODT will improve our understanding of the eco-evolutionary drivers of plant–insect interactions.