Quantitative comparison between the rhizosphere effect of Arabidopsis thaliana and co-occurring plant species with a longer life history

Abstract

As a model for genetic studies, Arabidopsis thaliana (Arabidopsis) offers great potential to unravel plant genome-related mechanisms that shape the root microbiome. However, the fugitive life history of this species might have evolved at the expense of investing in capacity to steer an extensive rhizosphere effect. To determine whether the rhizosphere effect of Arabidopsis is different from other plant species that have a less fugitive life history, we compared the root microbiome of Arabidopsis to eight other, later succession plant species from the same habitat. The study included molecular analysis of soil, rhizosphere, and endorhizosphere microbiome both from the field and from a laboratory experiment. Molecular analysis revealed that the rhizosphere effect (as quantified by the number of enriched and depleted bacterial taxa) was ~35% lower than the average of the other eight species. Nevertheless, there are numerous microbial taxa differentially abundant between soil and rhizosphere, and they represent for a large part the rhizosphere effects of the other plants. In the case of fungal taxa, the number of differentially abundant taxa in the Arabidopsis rhizosphere is 10% of the other species’ average. In the plant endorhizosphere, which is generally more selective, the rhizosphere effect of Arabidopsis is comparable to other species, both for bacterial and fungal taxa. Taken together, our data imply that the rhizosphere effect of the Arabidopsis is smaller in the rhizosphere, but equal in the endorhizosphere when compared to plant species with a less fugitive life history.

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Fig. 1: Species relative abundances change over time.
Fig. 2: Alpha diversity and phylum-level taxonomy indicate a rhizosphere effect in all plant species.
Fig. 3: The Arabidopsis bacterial rhizosphere is substantially changed.
Fig. 4: A majority of highly abundant plant-enriched bacterial OTUs is shared with Arabidopsis.
Fig. 5: OTUs can be affected in only one or in multiple plant species.
Fig. 6: The rhizosphere effect on the fungal community.
Fig. 7: The rhizosphere effect can be reconstituted in a laboratory experiment.
Fig. 8: Quantitative comparison of the Arabidopsis rhizosphere effect.

Data availability

The raw sequencing reads are available online under accession number PRJNA605923. The OTU table and custom R scripts are available upon request.

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Acknowledgements

We would like to thank Nicole van Dam for pointing out the Mossel area to study Arabidopsis in the most ecologically relevant setting. We would like to thank Victor Carrion for valuable help with the statistical tests using metagenomeSeq package in R. We would like to acknowledge Ruben Garrido-Oter for making his custom R-scripts publicly available. Thanks to Liesje Mommer for valuable comments on the fungal data. Furthermore, we would like to thank Elizabeth Prins and Aliesje Schneijderberg for helping with the harvesting of the field experiment.

Funding

This research was funded by ERC grant number 3100000843.

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MS, XC, and CF executed the field and lab experiment. MdH, RvV, and LS constructed and implemented the bioinformatics pipelines. MS conducted in silico analyses. RH measured the relative area cover of Arabidopsis. MB and WvdP provided species abundance data and helped setting up this study. MS, MB, RG, and TB wrote the manuscript.

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Correspondence to Xu Cheng or Ton Bisseling.

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Schneijderberg, M., Cheng, X., Franken, C. et al. Quantitative comparison between the rhizosphere effect of Arabidopsis thaliana and co-occurring plant species with a longer life history. ISME J 14, 2433–2448 (2020). https://doi.org/10.1038/s41396-020-0695-2

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