Whole-genome duplication but not domestication shapes phyllosphere microbiome resilience across angiosperms globally

Whole-genome duplication (polyploidization) and domestication are two of the most influential evolutionary forces driving plant diversity, yet whether they exert consistent effects on plant-associated microbiomes remains poorly understood. Understanding these effects is critical, as phyllosphere and rhizosphere microbiomes mediate plant resilience to environmental change. Analyzing over 7,000 microbiomes from 250 plant species, we show that polyploidy, not domestication, consistently shapes phyllosphere microbiome properties across angiosperms globally. Polyploid phyllosphere microbial networks exhibited significantly higher modularity with greater redundancy and enrichment of functions involved in abiotic stress mitigation. Notably, these effects were conserved across both prokaryotic and fungal communities, a cross-kingdom consistency not commonly reported in plant microbiome research. These properties collectively point to phyllosphere microbiomes associated with greater stability in polyploids. Domestication did not erode these polyploidy-associated properties, as domesticated polyploids retained phyllosphere microbial community richness levels comparable to wild plants. In contrast, rhizosphere microbiome properties were driven primarily by geographic variables, suggesting that belowground plant-associated microbial communities are environment-specific rather than plant genome-mediated. Taken together, these findings reveal polyploidy as a general evolutionary force linking plant genome evolution to phyllosphere microbiome stability, suggesting an overlooked ecological advantage that may contribute to polyploid persistence and success under environmental change.