Climate-driven divergence in plant-microbiome interactions generates range-wide variation in bud break phenology

Ian Ware et al. use reciprocal plant population by soil location feedback experiments to show how the soil microbiomes of the narrowleaf cottonwood are influenced by genetic and environmental variation, and how these factors affect foliar phenology. They find a landscape-level feedback between tree populations and their associated soil microbial counterparts. This study contributes to the understanding of the interplay between soil, climate, plant and microbial populations with climate warming. Soil microbiomes are rapidly becoming known as an important driver of plant phenotypic variation and may mediate plant responses to environmental factors. However, integrating spatial scales relevant to climate change with plant intraspecific genetic variation and soil microbial ecology is difficult, making studies of broad inference rare. Here we hypothesize and show: 1) the degree to which tree genotypes condition their soil microbiomes varies by population across the geographic distribution of a widespread riparian tree, Populus angustifolia; 2) geographic dissimilarity in soil microbiomes among populations is influenced by both abiotic and biotic environmental variation; and 3) soil microbiomes that vary in response to abiotic and biotic factors can change plant foliar phenology. We show soil microbiomes respond to intraspecific variation at the tree genotype and population level, and geographic variation in soil characteristics and climate. Using a fully reciprocal plant population by soil location feedback experiment, we identified a climate-based soil microbiome effect that advanced and delayed bud break phenology by approximately 10 days. These results demonstrate a landscape-level feedback between tree populations and associated soil microbial communities and suggest soil microbes may play important roles in mediating and buffering bud break phenology with climate warming, with whole ecosystem implications.

Automated summary

The study demonstrates how the soil microbiomes of narrowleaf cottonwood are influenced by genetic and environmental factors, affecting foliar phenology. It also shows a landscape-level feedback between tree populations and soil microbes, suggesting the importance of soil microbes in mediating plant responses to climate warming. The research highlights the intricate interplay between soil, climate, plant genetics, and microbial populations at a broad geographic scale.