Host genetics shapes Pinus radiata phenotypic plasticity under drought and is linked with root-associated soil microbiome shifts

Under current and future climate scenarios, identifying drought-resistant tree species, tree genotypes, and beneficial interactions between trees and their root-associated soil microbiomes is becoming more imperative for maintaining tree health and sustaining increasingly vulnerable forests. We designed a genotype x soil x watering x time glasshouse experiment using Pinus radiata as a model tree to assess the magnitude of the effect of host genotype and root-associated soil microbiome on the phenotype response (functional traits, metabolome, nutrients) under drought. We identified the shikimate pathway as a critical metabolic pathway for Pinus radiata drought resistance, with the shikimic acid intermediate being one of the strongest drought signals, besides downstream metabolites such as flavonoids and phenylpropanoids. Overall, we found that the host genotype diversity was a key actor in the observed phenotype response of P. radiata to drought. In contrast, the microbiome was attributed a minor supporting role. Contrary to our hypothesis, dry soils could not support drought-sensitive genotypes under drought stress. Instead, the drought-resistant genotype was able to leverage locally adaptive bacteria to match local selective drought pressures at the expense of tree growth. This highlights the significance of finding specific combinations of tree genotype and mutualistic microbial communities that would thrive under future environmental pressures. •Phenotypic plasticity of Pinus radiata detected in the metabolome.•Shikimate pathway identified as a major metabolic pathway of drought resistance.•Higher magnitude of host genotype effect compared with root microbiome effect.•Drought-resistant genotype able to recruit beneficial bacteria to face drought.