Benzoxazinoid-mediated microbiome feedbacks enhance Arabidopsis growth and defence

  1. Katja Stengele
  2. Lea Stauber
  3. Lisa Thoenen
  4. Henry Janse van Rensburg
  5. Viola D’Adda
  6. Klaus Schlaeppi

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Abstract

  • Plants modulate their surrounding microbiome via root exudates and such conditioned soil microbiomes feed back on the performance of the next generation of plants. How plants perceive altered soil microbiomes and modulate their performance in response to such microbiome feedbacks however remains largely unknown.

  • As tool to condition contrasting microbiomes in soil, we made use of two maize lines, which differ in their ability to exude benzoxazinoids. Based on these differentially conditioned soil microbiomes we have established a model system with Arabidopsis thaliana (Arabidopsis) to investigate the mechanisms of microbiome feedbacks.

  • Arabidopsis plants responding to the benzoxazinoid-conditioned soil microbiome grew better and were developmentally more advanced. Further, these plants harboured differential root bacterial communities, showed enhanced defence signatures in transcriptomes of their shoots and they were more resistant to the fungal pathogen Botrytis cinerea .

  • Intriguingly, Arabidopsis responded with both improved growth and enhanced defence to the benzoxazinoid-conditioned soil microbiome, and we found that this simultaneous increase of growth and defence was mediated by priming of the defences. Further advancing our basic understanding how plants respond to soil microbiomes and mediate their feedbacks is particularly important for the goal to improve crops so they can benefit from their soil microbiome.

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  1. PREreview

    This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/14057417.

    Review of Preprint:  Benzoxazinoid-mediated microbiome feedbacks enhance Arabidopsis  growth and defense 

    By J.M. D'Amobrosio, S. Frecha, S. Lorenzani, J. Benjamín, E. Perk, R. Pantaleno, P. Schiel, N. Tebez, A.M. Laxalt

    Why selected the pre-print as part of our first experience reviewing a pre-print in the just founded pre-print club at the IIB, Mar del Plata, Argentina. We are learning how to do it, and in doing so…we hope to contribute to improve the MS.

    doi: https://doi.org/10.1101/2024.10.21.619081

    Summary

    The article focuses on how benzoxazinoid (BX) secondary metabolites exuded by maize influence soil microbiota, which in turn affects the growth and defenses of Arabidopsis thaliana. The study used soils conditioned with maize that either exudes or does not exude benzoxazinoids to observe how Arabidopsis responds in terms of growth and resistance to pathogens, specifically against the fungus Botrytis cinerea.

    Introduction

    The authors provide a context for the study, yet several areas would benefit from clarification and additional references. Specifically:

    • Line 84: The origin of APO and the specific microorganisms involved in its metabolism are not clearly defined. Providing more detail on these aspects would enhance the reader's understanding of the study's relevance.

    • Additionally, the potential benefits to maize for releasing exudates are implied but not explicitly discussed. The authors should clarify if these exudates inhibit the growth of other species, or if they provide some other selective advantage.

    Results

    Figure 1

     Enhancing the clarity of the experimental design and the rationale behind the choice of representative experiment in the figure legend would help readers better understand the purpose and context of the data. Additionally, specifying the number of replicates in the figure legend would improve data transparency and assist readers in assessing the reliability of the results.

    For Panel E, a revised layout could better align with the overall data presentation. Lastly, to avoid potential misunderstandings, it may be beneficial to reserve terms like "trend" (Line 270) for statistically significant findings.

    Figure 2

    • For Fig. 2b, it would be helpful to label the x-axis with specific time points (days) and add units for the concentration measurements.

    • An interesting question arises regarding whether the BX-nat soil treatment could also receive exudate as part of the experimental setup. This could provide valuable comparative insights.

    Figure 3

    • The current conclusions drawn from Fig. 3 do not appear to be fully supported by the graphical data. For instance, Lines 313-315 state, "Together with the plant growth data (Fig. 2a), these experiments suggested that BXs in soil cause a differentiation of the root microbiotas and that these differential microbiotas – particularly the bacteria – would drive the differential growth of Arabidopsis." However, these observations are not readily apparent from the figure. The authors should either adjust this conclusion to reflect observable trends more accurately or provide additional evidence to substantiate it.

    Figure 4

    • No comments.

    Figure 5

    • Including a representative photograph of Arabidopsis infected with Botrytis would add a valuable visual context to the findings.

    • The small growth area in experiment IX is intriguing; it would be helpful to provide an explanation or hypothesis for this variation.

    • The differences in lesion area caused by the pathogen across experiments also stand out and merit further discussion. Additionally, unifying the plant age between the main text and figure legend in Materials and Methods would improve clarity.

    • Finally, the authors should clarify whether sterile soil was used in the infection experiments, as this detail would impact interpretation.

    Competing interests

    The authors declare that they have no competing interests.

  2. Version published to 10.1101/2024.10.21.619081 on bioRxiv