Benzoxazinoid-mediated microbiome feedbacks enhance Arabidopsis growth and defense

  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 this conditioned soil microbiome feeds back on the performance of the next generation of plants. How plants can perceive this altered microbiome and modulate their performance in response to such microbiome feedbacks however remains largely unknown. We made use of two maize lines, which differ in their ability to exude benzoxazinoids, to condition two contrasting soil microbiomes in the same starting soil. Based on these conditioned soils we have established a model system with Arabidopsis thaliana (Arabidopsis) to investigate the mechanisms of microbiome feedbacks. Arabidopsis plants grown on the benzoxazinoids conditioned soil developed larger rosettes, for which the soil microbiome was required. Arabidopsis roots also harbored differential bacterial communities. Further, these plants showed enhanced defense signatures in their shoot and were more resistant to the fungal pathogen Botrytis cinerea . We could establish Arabidopsis as a model to study benzoxazinoid-mediated microbiome feedbacks, which will allow future studies to investigate underlying mechanisms. Arabidopsis also responded with both improved growth and enhanced resistance to a complex benzoxazinoids conditioned microbiome, and we hypothesize that this simultaneous increase of growth and defense is mediated by priming of defenses.

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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 10.1101/2024.10.21.619081v1 on bioRxiv