Mineral geochemistry and mycorrhizal allocation define root architectural strategy during early vascular plant colonization

The emergence of vascular plants on land is one of evolution greatest triumphs. This success was contingent on the capacity of roots and their symbionts to acquire resources from exposed geology. However, how rock chemistry shapes plant root architectural strategies, and their return on investment during early ecosystem colonization remains poorly understood. Here we use a two-year mesocosm experiment with Bouteloua dactyloides grass and an arbuscular mycorrhizal symbiont, grown on four mineral substrates of contrasting composition, to show that rock geochemistry predictably determines root topological strategy, from herringbone architecture on nutrient-poor granite to dichotomous-like branching on nutrient-rich basalt. Substrate identity governed investment allocation between root complexity and biomass, with plants consolidating existing transport pathways as weathering-derived nutrients subsided. Traits associated with exploratory effort were generally decoupled from those related to biomass buildup. In basalt and rhyolite plants preferentially invested in complexity, generating the largest numbers of prospective tips for mining and biomass buildup; in granite, plants chose a surviving strategy, limiting branching to preserve biomass; while in schist, plants balanced biomass with complexity, extending growth on low investment, which increased tissue density. Surprisingly, mycorrhizal fungi did not alter the whole root system size, but reallocated investment between specific root orders, discouraging investment in embryonic roots in some substrates, and stimulating lateral expansion of the rooting system in others. This extends the functional balance mechanism from plant to the plant-fungus system. The extensive phenotypic plasticity of the root-mycorrhiza system shown here provides an evolutionary space for natural selection, which must have played a crucial role in the success of plants on land in the past, and is crucial for understanding plant ecological dynamics today.