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Local Plants, Not Soils, Are the Primary Source of Foliar Fungal Community Assembly in a C4 Grass

  • Plant Microbe Interactions
  • Published:
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Abstract

Microbial communities, like their macro-organismal counterparts, assemble from multiple source populations and by processes acting at multiple spatial scales. However, the relative importance of different sources to the plant microbiome and the spatial scale at which assembly occurs remains debated. In this study, we analyzed how source contributions to the foliar fungal microbiome of a C4 grass differed between locally abundant plants and soils across an abiotic gradient at different spatial scales. Specifically, we used source-sink analysis to assess the likelihood that fungi in leaves from Panicum hallii came from three putative sources: two plant functional groups (C4 grasses and dicots) and soil. We expected that physiologically similar C4 grasses would be more important sources to P. hallii than dicots. We tested this at ten sites in central Texas spanning a steep precipitation gradient. We also examined source contributions at three spatial scales: individual sites (local), local plus adjacent sites (regional), or all sites (gradient-wide). We found that plants were substantially more important sources than soils, but contributions from the two plant functional groups were similar. Plant contributions overall declined and unexplained variation increased as mean annual precipitation increased. This source-sink analysis, combined with partitioning of beta-diversity into nestedness and turnover components, indicated high dispersal limitation and/or strong environmental filtering. Overall, our results suggest that the source-sink dynamics of foliar fungi are primarily local, that foliar fungi spread from plant-to-plant, and that the abiotic environment may affect fungal community sourcing both directly and via changes to host plant communities.

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Data and Code Availability

Raw sample data, bioinformatic code, and R statistical code are available on GitHub 10.5281/zenodo.5076546 [50]. Raw sequence data have been deposited in NCBI Short Read Archive under BioProject PRJNA672680.

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Acknowledgements

For help with field and lab work, we thank Elise Connor, Tyler Johnson, and Mitch Sellers. Site access was kindly provided by Texas Ecolab, Texas State Parks and Wildlife, the Texas State Historical Association, the City of Austin, and the Ladybird Johnson Wildflower Center. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture (USDA). The USDA is an equal opportunity provider and employer.

Funding

Support for this project was provided by Texas Ecolab program to HG and CVH. In addition, CVH was supported by USDA Hatch (accession no. 1018688) and Department of Energy Genomic Sciences Program SFA (SCW1039) subaward from Lawrence Livermore National Lab. BKW was supported in part by the U.S. Department of Agriculture, Agricultural Research Service.

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Authors and Affiliations

  1. Department of Plant and Microbial Biology, North Carolina State University, 112 Derieux Place, Raleigh, NC, 27607, USA

    Briana K. Whitaker & Christine V. Hawkes

  2. USDA, Agricultural Research Service, National Center for Agricultural Utilization Research, Mycotoxin Prevention & Applied Microbiology Unit, 1815 N University St, Peoria, IL, 61604, USA

    Briana K. Whitaker

  3. Department of Integrative Biology, University of Texas Austin, Austin, TX, USA

    Hannah Giauque, Corey Timmerman, Nicolas Birk & Christine V. Hawkes

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  1. Briana K. Whitaker
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  2. Hannah Giauque
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  4. Nicolas Birk
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  5. Christine V. Hawkes
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Contributions

HG and CVH conceived of the ideas and designed the experiments. Fieldwork and labwork were carried out by HG and CT. BKW and NB analyzed data. BKW and CVH wrote the manuscript.

Corresponding author

Correspondence to Christine V. Hawkes.

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Whitaker, B.K., Giauque, H., Timmerman, C. et al. Local Plants, Not Soils, Are the Primary Source of Foliar Fungal Community Assembly in a C4 Grass. Microb Ecol 84, 122–130 (2022). https://doi.org/10.1007/s00248-021-01836-2

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