Specific and conserved patterns of microbiota-structuring by maize benzoxazinoids in the field

Cadot, Selma; Guan, Hang; Bigalke, Moritz; Walser, Jean‐Claude; Jander, Georg; Erb, Matthias; Heijden, Marcel van der; Schlaeppi, Klaus

doi:10.1101/2020.05.03.075135

Cited by 7 publications

(13 citation statements)

References 61 publications

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“…Our work complements recent research efforts to understand the effect of benzoxazinoids on plant-associated microbiota in soil (Cadot et al, 2020;Cotton et al, 2019;Kudjordjie et al, 2019;Neal et al, 2012). Ultimately, for in vitro SynCom systems to be a useful model for plant microbiota research, they should behave similarly to microbiota in soil.…”

Section: Stability Of Communities In Vitromentioning

confidence: 67%

“…Hu et al [17] found Flavobacterium depleted on the roots of BX-exuding plants and the surrounding soils when comparing wildtype and bx1 mutant plants. Extending these observations, Cadot et al [22] reported that Flavobacteriaceae were consistently depleted on roots of BX-producing plants, independent of soil type and location. Similarly, members of the Flavobacteriales family were more abundant on the roots of maize BX-synthesis mutants than on wildtype in another, independent study [20].…”

Section: Discussionmentioning

confidence: 90%

“…Since previous studies reported a substantial impact of plant-derived BX on soil microbiota Cotton et al, 2019;Kudjordjie et al, 2019;Cadot et al, 2020), we were interested in assessing if the reported effects could be recapitulated using reduced complexity communities in vitro. To understand which taxa drove the observed differences between treatments ( Figure 2), and if similar changes occurred upon APO treatment in the different communities, we estimated the fold-change in taxon abundance per SynCom and time point between APO-and BOA-treated samples as well as between APO and control, and between BOA and control ( Figure 3).…”

Section: Response Of Community-embedded Isolates To Bx Treatmentmentioning

confidence: 99%

“…For example, BX exudation by maize plants into the surrounding soil leads to conditioning of the microbiome, which in turn results in soil-memory effects that affect plants of the following sowing [17]. Another study showed that BX exudation specifically recruits beneficial pseudomonads to the rhizosphere [18–22].…”

Section: Introductionmentioning

confidence: 99%

“…For example, BX exudation by maize plants into the surrounding soil conditions the microbiome, which in turn results in soil-memory effects that affect plants of the following sowing (Hu et al, 2018). Other studies showed that BX exudation specifically recruits beneficial pseudomonads to the rhizosphere, whereas Comamonadaceae are often depleted by BX exudation (Cadot et al, 2020; Cotton et al, 2019; Kudjordjie et al, 2019; Neal et al, 2012; Schandry and Becker, 2020). Conversely, the presence and composition of the microbiota can alter BX chemistry.…”

Section: Introductionmentioning

confidence: 99%

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Plant-derived benzoxazinoids act as antibiotics and shape bacterial communities

Schandry

Jandrasits

Garrido‐Oter

et al. 2021

Preprint

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Plants synthesize and release specialized metabolites into their environment that can serve as chemical cues for other organisms. Metabolites that are released from the roots are important factors in determining which microorganisms will colonize the root and become part of the plant rhizosphere microbiota. Root exudates are often further converted by soil microorganisms, which can result in the formation of toxic compounds. How individual members of the plant rhizosphere respond to individual compounds and how the differential response of individual microorganisms contributes to the response of a microbial community remains unclear. Here, we investigated the impact of derivatives of one class of plant root exudates, benzoxazinoids, which are released by important crops such as wheat and maize, on a collection of 180 root-associated bacteria. We show that phenoxazine, derived from benzoxazinoids, inhibits the growth of root-associated bacteria in vitro in a strain-specific manner, with sensitive and resistant isolates in most of the studied clades. Synthetic bacterial communities that were assembled from only resistant isolates were more resilient to chemical perturbations than communities comprised of only sensitive members. Isolates that were shared between different communities revealed stable interactions, independent of the overall community composition. On the other hand, we could attribute differential community development to differences in interactions formed by closely related representatives of the same bacterial genus. Our findings highlight the fact that profiling isolate collections can aid the rational design of synthetic communities. Moreover, our data show that simplified in vitro community systems are able to recapitulate observations on the influence of metabolite exudation on the structure of root-associated communities, thus providing an avenue for reductionist explorations of the rhizosphere biology in defined, host-free settings.

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Section: Stability Of Communities In Vitromentioning

confidence: 67%

Section: Discussionmentioning

confidence: 90%

Section: Response Of Community-embedded Isolates To Bx Treatmentmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Plant-derived benzoxazinoids act as antibiotics and shape bacterial communities

Schandry

Jandrasits

Garrido‐Oter

et al. 2021

Preprint

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Synergistically promoting plant health by harnessing synthetic microbial communities and prebiotics

ur-Rehman

et al. 2021

iScience

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Soil-borne diseases cause serious economic losses in agriculture. Managing diseases with microbial preparations is an excellent approach to soil-borne disease prevention. However, microbial preparations often exhibit unstable effects, limiting their large-scale application. This review introduces and summarizes disease-suppressive soils, the relationship between carbon sources and the microbial community, and the application of human microbial preparation concepts to plant microbial preparations. We also propose an innovative synthetic microbial community assembly strategy with synergistic prebiotics to promote healthy plant growth and resistance to disease. In this review, a new approach is proposed to improve traditional microbial preparations; provide a better understanding of the relationships among carbon sources, beneficial microorganisms, and plants; and lay a theoretical foundation for developing new microbial preparations.

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Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals

Cadot

Gfeller

et al. 2021

Preprint

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Plant-soil feedbacks refer to effects on plants that are mediated by soil modifications caused by the previous plant generation. Maize conditions the surrounding soil by secretion of root exudates including benzoxazinoids (BXs), a class of bioactive secondary metabolites. Previous work found that a BX-conditioned soil microbiota enhances insect resistance while reducing biomass in the next generation of maize plants. Whether these BX-mediated and microbially driven feedbacks are conserved across different soils and response species is unknown. We found the BX-feedbacks on maize growth and insect resistance conserved between two arable soils, but absent in a more fertile grassland soil, suggesting a soil-type dependence of BX feedbacks. We demonstrated that wheat also responded to BX-feedbacks. While the negative growth response to BX-conditioning was conserved in both cereals, insect resistance showed opposite patterns, with an increase in maize and a decrease in wheat. Wheat pathogen resistance was not affected. Finally and consistent with maize, we found the BX-feedbacks to be cultivar specific. Taken together, BX-feedbacks affected cereal growth and resistance in a soil and genotype dependent manner. Cultivar-specificity of BX-feedbacks is a key finding, as it hides the potential to optimize crops that avoid negative plant-soil feedbacks in rotations.

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Specific and conserved patterns of microbiota-structuring by maize benzoxazinoids in the field

Cited by 7 publications

References 61 publications

Plant-derived benzoxazinoids act as antibiotics and shape bacterial communities

Plant-derived benzoxazinoids act as antibiotics and shape bacterial communities

Synergistically promoting plant health by harnessing synthetic microbial communities and prebiotics

Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals

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