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

Abstract

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.

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Data availability

Data consists of two curated spreadsheets of LC-MS output which gives the relative concentration of each metabolite in each sample and sufficient meta-data about the sample (one for soil samples and one for root samples), the raw spectra from the LC-MS output, as well as 10,956 EXCEL files associated with the 7 golden rules output (for each metabolite the program could solve for) which was sub sampled for the Van Krevelen diagrams shown here. All data is available on MetaboLights database.

Notes

  1. Here we use the notation soil rhizosphere metabolome, with the understanding that soil rhizosphere chemistry is a complex matrix that could encompass root exudates, microbial metabolomes and extra-cellular soil chemical processes.

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Acknowledgments

The authors would like to thank Ian Ware, Michael van Nuland, Philip Patterson, and Courtney Gorman for assistance in the field and greenhouse as well as Terrell Carter and Michaela Humby for their help in the lab. Thank you to Melissa Liotta and Shannon Bayliss for their help building figures. Thanks to Ken McFarland and Jeff Martin for their greenhouse expertise. We would like to acknowledge funding from The University of Tennessee, Department of Ecology and Evolutionary Biology.

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Contributions

LOM, HFC, SRC, JKB, and JAS formulated the initial questions. EDT, SPD, HFC, and SRC performed the chemical assays. LOM, SRB, EDT, HFC, and SRC performed the chemical analysis. LOM and SRB performed the statistical analyses. Writing was shared by all authors.

Corresponding author

Correspondence to Liam O. Mueller.

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Mueller, L.O., Borstein, S.R., Tague, E.D. et al. Populations of Populus angustifolia have evolved distinct metabolic profiles that influence their surrounding soil. Plant Soil 448, 399–411 (2020). https://doi.org/10.1007/s11104-019-04405-2

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Keywords

  • Co-inertia
  • Distance based redundancy analysis
  • LC-MS
  • Metabolomics
  • Orbitrap
  • Plant conditioning
  • Rhizosphere
  • Van Krevelen diagrams