Evaluating the legacy of drought exposure on root and rhizosphere bacterial microbiomes over two plant generations

Drought is a critical risk for staple crops like common bean (Phaseolus vulgaris L.). We conducted an experiment to understand the legacy effects of repeated drought exposure across plant generations on the root and rhizosphere microbiome of the common bean, hypothesizing that a legacy of exposure improves overall plant microbiome resilience. We profiled the bacterial microbiome using marker gene amplicon sequencing over two plant generations in a complete factorial design for two common bean genotypes, Red Hawk and Flavert. We performed parallel experiments for Red Hawk in two different countries using soils of Pays de la Loire, France, and Michigan, USA. Despite the clear and relatively consistent drought effects on the plant phenotypes, there was neither a strong response of the Red Hawk microbiomes to drought nor a notable legacy of drought exposure. For Flavert, there was a minor legacy drought effect for the second generation in the rhizosphere microbiome beta diversity, while its root had no legacy effect observed. This study demonstrates that below-ground plant microbiomes can be resistant to drought stress and that cross-generational legacy depends on soil origin and host genotype. Such parallel experiments across countries are useful to inform generalities and build theory toward prediction on microbiome responses to global change.IMPORTANCEDrought remains an important challenge in crop agriculture because of climate change, and plant microbiome management has potential to support plant resilience to drought. Here, we investigated the impact of drought and drought legacy across two generations on the root and rhizosphere microbiomes of the drought-susceptible legume common bean, a key staple food crop with production widely distributed across the Americas, Africa, Europe, and Asia, and which is of critical importance for food security in many of its production regions. Despite host plant decline with drought, the effects of drought on the microbiomes were either not observed, inconsistent, or weak, suggesting overall microbiome resistance and limited drought legacy. This work provides insights into how the stability of the below-ground plant microbiome can be driven by stress resistance, offering a different perspective on how the microbiome could be managed to support crops facing drought.