Towards unravelling the mechanisms of “clever” plant roots designing resilient microbiomes

“Plants actively shape their associated microbial communities by synthesizing bio-active substances. Despite the univocal evidence of plant genotype effects on microbiome assemblage, and that a repertoire of plant exudates including secondary metabolites unique for each plant genotype drives microbial assemblage, little research attention is directed towards the mechanisms involved”.

Published in Microbiology

Towards unravelling the mechanisms of “clever” plant roots designing resilient microbiomes
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BioMed Central
BioMed Central BioMed Central

Maize synthesized benzoxazinoids affect the host associated microbiome - Microbiome

Background Plants actively shape their associated microbial communities by synthesizing bio-active substances. Plant secondary metabolites are known for their signaling and plant defense functions, yet little is known about their overall effect on the plant microbiome. In this work, we studied the effects of benzoxazinoids (BXs), a group of secondary metabolites present in maize, on the host-associated microbial structure. Using BX knock-out mutants and their W22 parental lines, we employed 16S and ITS2 rRNA gene amplicon analysis to characterize the maize microbiome at early growth stages. Results Rhizo-box experiment showed that BXs affected microbial communities not only in roots and shoots, but also in the rhizosphere. Fungal richness in roots was more affected by BXs than root bacterial richness. Maize genotype (BX mutants and their parental lines) as well as plant age explained both fungal and bacterial community structure. Genotypic effect on microbial communities was stronger in roots than in rhizosphere. Diverse, but specific, microbial taxa were affected by BX in both roots and shoots, for instance, many plant pathogens were negatively correlated to BX content. In addition, a co-occurrence analysis of the root microbiome revealed that BXs affected specific groups of the microbiome. Conclusions This study provides insights into the role of BXs for microbial community assembly in the rhizosphere and in roots and shoots. Coupling the quantification of BX metabolites with bacterial and fungal communities, we were able to suggest a gatekeeper role of BX by showing its correlation with specific microbial taxa and thus providing insights into effects on specific fungal and bacterial taxa in maize roots and shoots. Root microbial co-occurrence networks revealed that BXs affect specific microbial clusters.

The above excerpt from our paper was the motivation behind this research work. The story began three years ago when we decided to conduct a quick study to explore the influence of plant defensive secondary metabolite, benzoxazinoids on the maize associated microbiomes. This idea was fostered by two researchers who had fallen in love with two extreme specialties of science; plant pathology and natural product chemistry and were supported by enthusiastic and energetic lab group members.

Fast forward, we had many discussions on the experimental design that will enable us to achieve our objective of profiling BXs effects on microbiomes at different stages of maize development. One key challenge that we had was the choice of growth system that will be appropriate for this study. Nevertheless, things worked out quite well when we settled on the rhizobox growth system. We setup the experiment in our open semi-field facility and thus the seedlings enjoyed the coruscating 2016 summer sunshine. Throughout the sample preparation and data analysis phases, we continuously discussed the progress of work! This was important for effective collaborative studies!

Data exploration stage came with new excitement as interesting results trickled in and we were enlivened with curiosity to probe the data into details. Overall, our work revealed the role of BXs as key modulators or “gatekeepers” during maize microbiome assemblage. This was further corroborated by network analysis, which showed that BXs affected specific microbial clusters of the microbiome. Moreover, we found that BXs negatively correlated with specific plant pathogens that are of great economic importance. We therefore suggest that the higher BX synthesis during the early development of maize and its effect on microbial communities might open new frontiers for maize breeding in the future.

Poster 1: Microbial network based on Spearman’s correlations in the roots of W22_1 and its mutant. OTUs are shown as nodes, and correlations as edges. Positive and negative correlations are shown with grey and red edges, respectively. Bacterial and fungal nodes are represented as square and circle symbols in the network, respectively. Indicator OTUs for bx1W22_1 and W22_1 are shown with a large and a medium node size while others are shown with small size to indicate the location of indicator species in overall network

 Reference:

Kudjordjie EN, Sapkota R, Steffensen SK, Fomsgaard IS, Nicolaisen M. Maize synthesized benzoxazinoids affect the host associated microbiome. Microbiome; 2019;1–17. 

https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-019-0677-7

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Harnessing plant microbiomes to improve performance and mechanistic understanding

This is a Cross-Journal Collection with Microbiome, Environmental Microbiome, npj Science of Plants, and npj Biofilms and Microbiomes. Please click here to see the collection page for npj Science of Plants and npj Biofilms and Microbiomes.

Modern agriculture needs to sustainably increase crop productivity while preserving ecosystem health. As soil degradation, climate variability, and diminishing input efficiency continue to threaten agricultural outputs, there is a pressing need to enhance plant performance through ecologically-sound strategies. In this context, plant-associated microbiomes represent a powerful, yet underexploited, resource to improve plant vigor, nutrient acquisition, stress resilience, and overall productivity.

The plant microbiome—comprising bacteria, fungi, and other microorganisms inhabiting the rhizosphere, endosphere, and phyllosphere—plays a fundamental role in shaping plant physiology and development. Increasing evidence demonstrates that beneficial microbes mediate key processes such as nutrient solubilization and uptake, hormonal regulation, photosynthetic efficiency, and systemic resistance to (a)biotic stresses. However, to fully harness these capabilities, a mechanistic understanding of the molecular dialogues and functional traits underpinning plant-microbe interactions is essential.

Recent advances in multi-omics technologies, synthetic biology, and high-throughput functional screening have accelerated our ability to dissect these interactions at molecular, cellular, and system levels. Yet, significant challenges remain in translating these mechanistic insights into robust microbiome-based applications for agriculture. Core knowledge gaps include identifying microbial functions that are conserved across environments and hosts, understanding the signaling networks and metabolic exchanges between partners, and predicting microbiome assembly and stability under field conditions.

This Research Topic welcomes Original Research, Reviews, Perspectives, and Meta-analyses that delve into the functional and mechanistic basis of plant-microbiome interactions. We are particularly interested in contributions that integrate molecular microbiology, systems biology, plant physiology, and computational modeling to unravel the mechanisms by which microbial communities enhance plant performance and/or mechanisms employed by plant hosts to assemble beneficial microbiomes. Studies ranging from controlled experimental systems to applied field trials are encouraged, especially those aiming to bridge the gap between fundamental understanding and translational outcomes such as microbial consortia, engineered strains, or microbiome-informed management practices.

Ultimately, this collection aims to advance our ability to rationally design and apply microbiome-based strategies by deepening our mechanistic insight into how plants select beneficial microbiomes and in turn how microbes shape plant health and productivity.

This collection is open for submissions from all authors on the condition that the manuscript falls within both the scope of the collection and the journal it is submitted to.

All submissions in this collection undergo the relevant journal’s standard peer review process. Similarly, all manuscripts authored by a Guest Editor(s) will be handled by the Editor-in-Chief of the relevant journal. As an open access publication, participating journals levy an article processing fee (Microbiome, Environmental Microbiome). We recognize that many key stakeholders may not have access to such resources and are committed to supporting participation in this issue wherever resources are a barrier. For more information about what support may be available, please visit OA funding and support, or email OAfundingpolicy@springernature.com or the Editor-in-Chief of the journal where the article is being submitted.

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Our understanding of the intricate relationship between the microbiome and reproductive health holds profound translational implications for fertility, pregnancy, and reproductive disorders. To truly advance this field, it is essential to move beyond descriptive and associative studies and focus on mechanistic research that uncovers the functional underpinnings of the host–microbiome interface. Such studies can reveal how microbial communities influence reproductive physiology, including hormonal regulation, immune responses, and overall reproductive health.

Recent advances have highlighted the role of specific bacterial populations in both male and female fertility, as well as their impact on pregnancy outcomes. For example, the vaginal microbiome has been linked to preterm birth, while emerging evidence suggests that gut microbiota may modulate reproductive hormone levels. These insights underscore the need for research that explores how and why these microbial influences occur.

Looking ahead, the potential for breakthroughs is immense. Mechanistic studies have the power to drive the development of microbiome-based therapies that address infertility, improve pregnancy outcomes, and reduce the risk of reproductive diseases. Incorporating microbiome analysis into reproductive health assessments could transform clinical practice and, by deepening our understanding of host–microbiome mechanisms, lay the groundwork for personalized medicine in gynecology and obstetrics.

We invite researchers to contribute to this Special Collection on Microbiome and Reproductive Health. Submissions should emphasize functional and mechanistic insights into the host–microbiome relationship. Topics of interest include, but are not limited to:

- Microbiome and infertility

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This Collection supports and amplifies research related to SDG 3, Good Health and Well-Being.

All submissions in this collection undergo the journal’s standard peer review process. As an open access publication, this journal levies an article processing fee (details here). We recognize that many key stakeholders may not have access to such resources and are committed to supporting participation in this issue wherever resources are a barrier. For more information about what support may be available, please visit OA funding and support, or email OAfundingpolicy@springernature.com or the Editor-in-Chief.

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