Recent advances in the role of plant metabolites in shaping the root microbiome [version 1; peer review: 3 approved]

F1000Research 2020, 9(F1000 Faculty Rev):151 Last updated: 01 APR 2022 REVIEW Recent advances in the role of plant metabolites in shaping the root microbiome [version 1; peer review: 3 approved] Richard P. Jacoby, Li Chen, Melina Schwier, Anna Koprivova, Stanislav Kopriva Institute for Plant Sciences, Centre of Excellence on Plant Sciences (CEPLAS), University of Cologne, Cologne, 50674, Germany v1 First published: 26 Feb 2020, 9(F1000 Faculty Rev):151 https://doi.org/10.12688/f1000research.21796.1 Open Peer Review Latest published: 26 Feb 2020, 9(F1000 Faculty Rev):151 https://doi.org/10.12688/f1000research.21796.1 Approval Status 1 Abstract The last decade brought great progress in describing the repertoire of microbes associated with plants and identifying principles of their interactions. Metabolites exuded by plant roots have been considered candidates for the mechanisms by which plants shape their root microbiome. Here, we review the evidence for several plant metabolites affecting plant interaction with microbes belowground. We also discuss the development of new approaches to study the mechanisms of such interaction that will help to elucidate the metabolic networks in the rhizosphere. Keywords synthetic community, GWAS, microbiome, Arabidopsis, plant microbe interactions, exometabolomics, plant, plant metabolites 2 3 version 1 26 Feb 2020 Faculty Reviews are review articles written by the prestigious Members of Faculty Opinions. The articles are commissioned and peer reviewed before publication to ensure that the final, published version is comprehensive and accessible. The reviewers who approved the final version are listed with their names and affiliations. 1. Fabrice Roux, LIPM, Université de Toulouse, Institut National de Recherche en Agriculture, Alimentation et Environnement, Centre National de la Recherche Scientifique, Castanet, Tolosan, France 2. Philip Poole, University of Oxford, Oxford, UK 3. Corné Pieterse, Utrecht University, Utrecht, The Netherlands Any comments on the article can be found at the end of the article. Page 1 of 7 F1000Research 2020, 9(F1000 Faculty Rev):151 Last updated: 01 APR 2022 Corresponding author: Stanislav Kopriva () Author roles: Jacoby RP: Writing – Original Draft Preparation, Writing – Review & Editing; Chen L: Writing – Original Draft Preparation, Writing – Review & Editing; Schwier M: Writing – Original Draft Preparation, Writing – Review & Editing; Koprivova A: Writing – Original Draft Preparation, Writing – Review & Editing; Kopriva S: Conceptualization, Writing – Original Draft Preparation, Writing – Review & Editing Competing interests: No competing interests were disclosed. Grant information: The authors are funded by the Deutsche Forschungsgemeinschaft (DFG, the German Research Foundation) under Germany’s Excellence Strategy (EXC-Nummer 2048/1, project 390686111 to SK and AK), by a Humboldt Research Fellowship, and previously by a Horizon 2020 Marie Curie Sklodowska Action project (705808 – PINBAC to RPJ) and within the DFG SPP 2125 DECRyPT (to LC and MS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2020 Jacoby RP et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. How to cite this article: Jacoby RP, Chen L, Schwier M et al. Recent advances in the role of plant metabolites in shaping the root microbiome [version 1; peer review: 3 approved] F1000Research 2020, 9(F1000 Faculty Rev):151 https://doi.org/10.12688/f1000research.21796.1 First published: 26 Feb 2020, 9(F1000 Faculty Rev):151 https://doi.org/10.12688/f1000research.21796.1 Page 2 of 7 F1000Research 2020, 9(F1000 Faculty Rev):151 Last updated: 01 APR 2022 Introduction Plants in their natural environment are in constant interaction with diverse microorganisms. Whereas some microbes harm plants and trigger their defense reaction, others are beneficial for plant performance. Therefore, interactions between plant roots and rhizosphere microbiome are critical for plant fitness in an ambient environment. The technical innovations in cultivation of soil microbes and in sequencing technologies resulted in major biological breakthroughs in our understanding of plant microbiota1. The taxonomical composition of root bacterial microbiome is largely stable and is controlled by the soil and by plant genotype2–4. Indeed, plants produce a plethora of bioactive secondary metabolites and it has often been speculated that these molecules play an active role in shaping the rhizosphere microbiome5,6. However, this assumption was largely theoretical because relatively few studies defined which specific plant metabolites exert beneficial or antagonistic effects on distinct microbial strains. This situation is beginning to change since several new studies over the last five years have clearly illustrated how the plant microbiome can be shaped by the direct effects of specific metabolites7–9. The composition of root exudates varies not only among different plant species but also within different natural populations of the same species, which provides means to identify metabolites crucial for the interaction with the microbiota. In addition, the root exudates are affected by environment, particularly biotic factors10–12. Other tools and approaches have been developed to dissect the mechanisms of communication between plants and their microbiome. This review will summarize recent progress in the identification of metabolites involved in plant–microbe interactions, provide a set of the most important open questions, and propose ways that these can be addressed and answered. Metabolites involved in communication between plants and root microbiota The metabolites shaping plant microbiota belong to diverse classes. For example, the phenolic compounds coumarins are found across a wide variety of plant species and are relatively abundant in the rhizosphere where they have a well-characterized role in iron acquisition. However, two recent studies have independently shown that coumarins also play a key role in modulating root microbiome composition. Specifically, Stringlis et al.7 showed that coumarin-deficient Arabidopsis mutants recruit a different set of taxa to their rhizosphere microbiome. This seems to be partially mediated via strain-specific antimicrobial effects because one particular coumarin, scopoletin, exerts toxicity against two fungal pathogens but not against two commensal bacteria. Using synthetic community (SynCom) inoculations, Voges et al.9 show that the abundance of a Pseudomonas strain is significantly higher in coumarindeficient Arabidopsis mutants compared with wild-type plants. The mechanistic basis of this phenomenon seems to involve redox-mediated microbial toxicity be (...truncated)