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Plant specialized metabolites as drivers of plant-microbe interactions
Plant specialized metabolites as drivers of plant-microbe interactions
Plant specialized metabolites are important factors in shaping plant interactions with their microbiome, by influencing microbial colonization and survival on the host as well as bacterial community assembly. While metabolites are being secreted during the whole lifetime of a plant, these chemicals and their degradation products can remain stable in the soil for many years, impacting soil microbial composition and consequently subsequent plant generations, a process termed plant-soil feedback (Gfeller et al., 2023; Macías et al., 2004). Understanding the processes that dictate plant-soil feedback and microbiome assembly is critical for the establishment of efficient alternatives to conventional agriculture, such as crop rotations or microbial inoculants (Haskett et al., 2021). In this thesis, I performed a large computational analysis aiming at comparing the extended Resistance/Nodulation/Cell Division (RND) antiporter repertoire of plant- colonizing bacteria, in an effort to understand the role of multidrug efflux pumps in bacterial detoxification and adaptation to plant specialized metabolites. This broad scale analysis revealed organ-specific functionalization of RND antiporters and of recent gene transfer events, but did not find any conserved motif that could be linked to substrate-binding channel specificity. In a complementary analysis, I used plant associated bacterial mutants lacking RND antiporter homologues and found homologues responsible for the export of the legacy chemical 2-aminophenoxazin-3-one (APO), indicative of a specialization of these transporters for the export of specific metabolites. This work further examined the influence of soil legacy chemicals on bacteria-bacteria interactions, using the benzoxazinoids 2-benzoxazolinone (BOA) and APO. I show that the chemical environment has an effect on inter-bacterial competition, shifting the outcome from coexistence to inhibition. In order to assess whether these findings can be recapitulated in the presence of a host, I performed a large-scale meta-transcriptomic analysis of Arabidopsis thaliana colonized by single bacteria and bacterial pairs in the presence of APO. I found that the APO modulates plant defence responses, in particular the jasmonate signalling pathway. This effect is however restricted to the presence of a single isolate and disappears with increased microbial diversity, demonstrating the importance of deconstructing complex interactions to understand fine-tuned processes involved in plant-microbe interactions in varying chemical environments. Together, the findings presented in this thesis provide a multifaceted perspective on how soil legacy chemicals influence bacterial detoxification mechanisms, microbial community dynamics and plant responses to bacterial inoculation. This work further highlights the importance of soil legacy as a significant player in plant-microbe interactions, and provides new insights into factors to be considered for designing resilient sustainable agricultural practices.
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Rouyer, Liza
2026
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Rouyer, Liza (2026): Plant specialized metabolites as drivers of plant-microbe interactions. Dissertation, LMU München: Faculty of Biology
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Abstract

Plant specialized metabolites are important factors in shaping plant interactions with their microbiome, by influencing microbial colonization and survival on the host as well as bacterial community assembly. While metabolites are being secreted during the whole lifetime of a plant, these chemicals and their degradation products can remain stable in the soil for many years, impacting soil microbial composition and consequently subsequent plant generations, a process termed plant-soil feedback (Gfeller et al., 2023; Macías et al., 2004). Understanding the processes that dictate plant-soil feedback and microbiome assembly is critical for the establishment of efficient alternatives to conventional agriculture, such as crop rotations or microbial inoculants (Haskett et al., 2021). In this thesis, I performed a large computational analysis aiming at comparing the extended Resistance/Nodulation/Cell Division (RND) antiporter repertoire of plant- colonizing bacteria, in an effort to understand the role of multidrug efflux pumps in bacterial detoxification and adaptation to plant specialized metabolites. This broad scale analysis revealed organ-specific functionalization of RND antiporters and of recent gene transfer events, but did not find any conserved motif that could be linked to substrate-binding channel specificity. In a complementary analysis, I used plant associated bacterial mutants lacking RND antiporter homologues and found homologues responsible for the export of the legacy chemical 2-aminophenoxazin-3-one (APO), indicative of a specialization of these transporters for the export of specific metabolites. This work further examined the influence of soil legacy chemicals on bacteria-bacteria interactions, using the benzoxazinoids 2-benzoxazolinone (BOA) and APO. I show that the chemical environment has an effect on inter-bacterial competition, shifting the outcome from coexistence to inhibition. In order to assess whether these findings can be recapitulated in the presence of a host, I performed a large-scale meta-transcriptomic analysis of Arabidopsis thaliana colonized by single bacteria and bacterial pairs in the presence of APO. I found that the APO modulates plant defence responses, in particular the jasmonate signalling pathway. This effect is however restricted to the presence of a single isolate and disappears with increased microbial diversity, demonstrating the importance of deconstructing complex interactions to understand fine-tuned processes involved in plant-microbe interactions in varying chemical environments. Together, the findings presented in this thesis provide a multifaceted perspective on how soil legacy chemicals influence bacterial detoxification mechanisms, microbial community dynamics and plant responses to bacterial inoculation. This work further highlights the importance of soil legacy as a significant player in plant-microbe interactions, and provides new insights into factors to be considered for designing resilient sustainable agricultural practices.