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Drought legacy in rhizosphere bacterial communities alters subsequent plant performance

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Abstract

Purpose

Rhizosphere bacterial communities (‘rhizobacteria’) can mediate plant-soil feedbacks that enhance plant drought tolerance, but the composition and ecological characteristics of these populations are poorly understood. We investigated the impact of drought on rhizobacteria communities and the effect of propagating drought-impacted communities on the drought tolerance of naïve plants in a two-phase experiment.

Methods

We tested whether propagating rhizosphere soils from drought-stressed shrub willow (Salix purpurea), or continuously watered controls, affected the performance of a subsequent generation of droughted plants. The impacts of drought on rhizobacteria and plant fitness were evaluated using 16S rRNA gene sequencing and measures of plant growth (root mass and stem length etc.) and stress (abscisic acid, osmolality). Uninoculated reference plants were used to isolate the effects of inoculation.

Results

Drought had a significant and lasting impact on the structure of rhizobacterial communities, characterized by increased populations of Actinobacteria (Acidimicrobiia, Thermoleophilia and Micrococcaceae). Foliar osmolality was significantly higher in plants receiving drought-selected communities relative to uninoculated controls, but no significant differences in plant growth were observed. Inoculation with rhizosphere soil from watered controls significantly reduced plant growth. The rhizosphere of watered control plants was dominated by Proteobacteria and Bacteroidetes.

Conclusions

Our findings demonstrate that plants are affected by the legacy effects of drought on the rhizosphere microbiome. This drought legacy was propagated and persisted throughout nine weeks of plant growth, independent of prevailing water stress. Drought-impacted rhizospheres had larger populations of desiccation-tolerant (ex. Arthrobacter) and putatively endophytic taxa (ex. Rhizobium) with established plant growth promoting capabilities.

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Data availability

Accessioned at the NCBI under BioProject PRJEB41348.

Abbreviations

16S rRNA gene:

16S small subunit ribosomal RNA gene.

PCR:

Polymerase chain reaction

DEA buffer:

Diethanolamine buffer

PPFD:

Photosynthetic photon flux density

ABA:

Abscisic acid

E-phase:

Establishment phase, where plants are exposed to the first drought cycle.

T-phase:

Testing phase, where plants are inoculated with soils from the E-phase and exposed to a second drought cycle.

DRY:

Plants exposed to drought cycle treatment

WET:

Well-watered, control plants

REF:

Uninoculated sterile treatment

D:

Plants exposed to a second drought cycle in T-phase

C:

Plants continually well-watered in T-phase

References

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Acknowledgements

We would like to thank Larry Smart and his research group for providing plant material, growing advice and access to plantings; Emily Detrick and the Cornell Botanic Gardens for allowing us to collect soil; Hannah Swegarden and Zachary Stansell for collecting and transporting plant materials and soil, and Tim Setter for ABA assays.

Funding

Funding was provided by the Sustainable Biodiversity Fund from the Atkinson Center for a Sustainable Future and the Schmittau-Novak small grants program the School of Integrative Plant Science to JMU.

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Authors and Affiliations

Authors

Contributions

JMU, RCW, DHB and TLB conceived and designed experiments. JMU performed the experiments. RCW and JMU analyzed the data and wrote the manuscript with contributions from all authors.

Corresponding author

Correspondence to Taryn L. Bauerle.

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All authors consent to the publication of this work in Plant and Soil.

Conflicts of interest/Competing interests

The authors report no conflict of interest.

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Responsible Editor: Ricardo Aroca

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Munoz-Ucros, J., Wilhelm, R.C., Buckley, D.H. et al. Drought legacy in rhizosphere bacterial communities alters subsequent plant performance. Plant Soil 471, 443–461 (2022). https://doi.org/10.1007/s11104-021-05227-x

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  • DOI: https://doi.org/10.1007/s11104-021-05227-x

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