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Controlled natural selection of soil microbiome through plant-soil feedback confers resistance to a foliar pathogen

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Abstract

Background and aims

The rhizosphere microbiome has been shown to contribute to nutrient acquisition, protection against biotic and abiotic stresses and, ultimately, to changes in the development and physiology of plants. Here, using a controlled natural selection approach, we followed the microbial dynamics in the soil of Arabidopsis thaliana plants infected with the foliar pathogen Pseudomonas syringae DC3000 (Pst).

Methods

Plants were iteratively cultivated on a pasteurised soil inoculated with the soil microbial community of the previous iteration isolated from the rhizosphere of plants infected with Pst (pst-line) or not (mock-line). Modification of soil microbial communities was assessed through an amplicon-based metagenomic analysis targeting bacterial and fungal diversity. Plant fitness and transcript abundance of stress hormone related genes were also analysed.

Results

At the tenth and eleventh iterations respectively, we observed a reduction in disease severity of 81% and 85% in pst-lines as compared to mock-lines. These changes were associated with (i) an early induction of defence mechanisms mediated by salicylic acid, in pst-line as compared to mock-line, shown by the decrease in transcript abundance of salicylic acid related genes, whereas jasmonic acid, ethylene or abscisic acid related genes remained unchanged and (ii) a shift in soil bacterial, and not in fungal, composition.

Conclusions

Our study suggests that these changes in soil bacterial composition are mediated by plant-soil feedback in response to Pst and resulted in an activation of SA-related immune response in the plant. This supports the concept of applying plant-soil feedbacks to enhance soil suppressiveness against foliar pathogens.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

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Acknowledgements

We thank Sophie Michon-Coudouel and Romain Causse-Védrine from the EcogenO Platform (OSUR, France) for the preparation of the sequençing libraries and the sequencing. We are also grateful to the genotoul bioinformatics platform Toulouse Occitanie (Bioinfo Genotoul, https://doi.org/10.15454/1.5572369328961167E12) for providing computing resources, to Dr. Aleš Hanč from the Czech University of Life Sciences (Prague), for providing the vermicompost and to Pr. Anne Repellin from iEES-Paris, for English language editing and comments on the manuscript.

Funding

ER and RPF benefitted from an EC2CO initiative funding from CNRS. This work was also supported by the European Regional Development Fund, Project “Centre for Experimental Plant Biology” [grant no. CZ.02.1.01/0.0/0.0/16_019/0000738] and grant from the Contact Mobility - Barrande Program (PHC action) awarded to LB and RPF.

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Authors and Affiliations

Authors

Contributions

TK, LB, ER and RPF conceived and designed the study. TK and BJ performed the experiment. CM performed the soil DNA extraction and sequencing. RPF analysed the data. TK, MB, SJ, ER and RPF interpreted the data. TK, ER and RPF wrote the first manuscript and all authors contributed to the revision of the manuscript.

Corresponding author

Correspondence to Ruben Puga-Freitas.

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Competing interests

The authors have no relevant financial or non-financial interests to disclose.

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Responsible Editor: Jonathan Richard De Long.

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Kalachova, T., Jindřichová, B., Burketová, L. et al. Controlled natural selection of soil microbiome through plant-soil feedback confers resistance to a foliar pathogen. Plant Soil 485, 181–195 (2023). https://doi.org/10.1007/s11104-022-05597-w

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  • DOI: https://doi.org/10.1007/s11104-022-05597-w

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