Populations of Populus angustifolia have evolved distinct metabolic profiles that influence their surrounding soil

Aims Plant-microbial-soil interactions are key to understanding plant community succession, invasion success, patterns of biodiversity and aspects of ecosystem function. Yet root and rhizosphere chemistry is highly complex, and little is known about natural variation across environmental gradients. Variation in tree species root chemical phenotypes should alter how rhizosphere microbes respond, showing a plant conditioning effect on the chemical makeup of the soil. Here, we used metabolomics to assess bulk small molecule profiles addressing the hypothesis that genetic variation across a species range would result in varying metabolic profiles in roots and surrounding soil. Methods Using UPLC-HRMS we assessed the small molecule profile of root tissue and surrounding rhizosphere soil from 5-year old plant clones collected from six populations of Populus angustifolia across the western U.S., grown in a common environment. Results Population-level variation was found in over 12,000 root metabolomes and over 5000 soil organic compounds across the populations. Redundancy analysis of over twelve thousand metabolites suggests that plant population origin can account for up to 36% of the variation in roots and 30% of the variation in rhizosphere soil chemistry. Co-inertia analysis indicates that variation in root metabolite profiles explains 15% of the variation in paired soil samples. Conclusion Distinct populations have evolved different root tissue metabolomes. The difference in root metabolites across populations altered the rhizosphere soil composition, creating variable soil chemical communities from a homogenous starting condition. This suggests that intra-specific plant conditioning of soil varies by plant population.