Co‐evolution within the plant holobiont drives host performance

EMBO Reports, Journal Year: 2023, Volume and Issue: 24(9)

Published: July 20, 2023

Plants interact with a diversity of microorganisms that influence their growth and resilience, they can therefore be considered as ecological entities, namely "plant holobionts," rather than singular organisms. In plant holobiont, the assembly above- belowground microbiota is ruled by host, microbial, environmental factors. Upon microorganism perception, plants activate immune signaling resulting in secretion factors modulate composition. Additionally, metabolic interdependencies antagonism between microbes are driving forces for community assemblies. We argue complex plant-microbe intermicrobial interactions have been selected during evolution may promote survival fitness associated holobionts. As part this process, evolved metabolite-mediated strategies to selectively recruit beneficial microbiota. Some these members show host-adaptation, from which mutualism rapidly arise. also co-evolved antagonistic activities restrict proliferation high pathogenic potential prevent disease development. Co-evolution within holobionts thus ultimately drives performance.

Language: Английский

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Deep discovery informs difficult deployment in plant microbiome science

Cell, Journal Year: 2023, Volume and Issue: 186(21), P. 4496 - 4513

Published: Oct. 1, 2023

Plant-associated microbiota can extend plant immune system function, improve nutrient acquisition and availability, alleviate abiotic stresses. Thus, naturally beneficial microbial therapeutics are enticing tools to productivity. The basic definition of across species ecosystems, combined with the development reductionist experimental models manipulation phenotypes microbes, has fueled interest in its translation agriculture. However, great majority microbes exhibiting plant-productivity traits lab greenhouse fail field. Therapeutic must reach détente, establishment uneasy homeostasis, system, invade heterogeneous pre-established plant-associated communities, persist a new potentially remodeled community. Environmental conditions alter community structure thus impact engraftment therapeutic microbes. We survey recent breakthroughs, challenges, opportunities translating from

Language: Английский

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Strategies for tailoring functional microbial synthetic communities

The ISME Journal, Journal Year: 2024, Volume and Issue: 18(1)

Published: Jan. 1, 2024

Abstract Natural ecosystems harbor a huge reservoir of taxonomically diverse microbes that are important for plant growth and health. The vast diversity soil microorganisms their complex interactions make it challenging to pinpoint the main players life support functions can provide plants, including enhanced tolerance (a)biotic stress factors. Designing simplified microbial synthetic communities (SynComs) helps reduce this complexity unravel molecular chemical basis interplay specific microbiome functions. While SynComs have been successfully employed dissect or reproduce microbiome-associated phenotypes, assembly reconstitution these often based on generic abundance patterns taxonomic identities co-occurrences but only rarely informed by functional traits. Here, we review recent studies designing reveal common principles discuss multidimensional approaches community design. We propose strategy tailoring design integration high-throughput experimental assays with strains computational genomic analyses capabilities.

Language: Английский

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Sugar transporters spatially organize microbiota colonization along the longitudinal root axis of Arabidopsis

Cell Host & Microbe, Journal Year: 2024, Volume and Issue: 32(4), P. 543 - 556.e6

Published: March 12, 2024

Plant roots are functionally heterogeneous in cellular architecture, transcriptome profile, metabolic state, and microbial immunity. We hypothesized that axial differentiation may also impact spatial colonization by root microbiota along the axis. developed two growth systems, ArtSoil CD-Rhizotron, to grow then dissect Arabidopsis thaliana into three segments. demonstrate distinct endospheric rhizosphere bacterial communities colonize segments, supporting hypothesis of Root metabolite profiling each segment reveals differential enrichment specificity. Bioinformatic analyses GUS histochemistry indicate microbe-induced accumulation SWEET2, 4, 12 sugar uniporters. Profiling segments from sweet mutants shows altered profiles reorganization microbiota. This work interdependency between metabolites contribution SWEETs diversity stability ecosystem.

Language: Английский

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Bacterial tolerance to host-exuded specialized metabolites structures the maize root microbiome

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(44)

Published: Oct. 25, 2023

Plants exude specialized metabolites from their roots, and these compounds are known to structure the root microbiome. However, underlying mechanisms poorly understood. We established a representative collection of maize bacteria tested tolerance against benzoxazinoids (BXs), dominant bioactive in exudates plants. In vitro experiments revealed that BXs inhibited bacterial growth strain- compound-dependent manner. Tolerance selective antimicrobial depended on cell wall structure. Further, we found native isolated tolerated better compared nonhost Arabidopsis bacteria. This finding suggests adaptation host plant. Bacterial 6-methoxy-benzoxazolin-2-one (MBOA), most abundant metabolite rhizosphere, correlated significantly with abundance BX-exuding roots. Thus, strain-dependent largely explained pattern Abundant generally MBOA, while low microbiome members were sensitive this compound. Our findings reveal plant is an important competence determinant for colonization. propose root-derived mechanism determining host-specific microbial communities.

Language: Английский

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Unraveling plant–microbe interactions: can integrated omics approaches offer concrete answers?

Journal of Experimental Botany, Journal Year: 2023, Volume and Issue: 75(5), P. 1289 - 1313

Published: Nov. 9, 2023

Abstract Advances in high throughput omics techniques provide avenues to decipher plant microbiomes. However, there is limited information on how integrated informatics can help deeper insights into plant–microbe interactions a concerted way. Integrating multi-omics datasets transform our understanding of the microbiome from unspecified genetic influences interacting species specific gene-by-gene interactions. Here, we highlight recent progress and emerging strategies crop research review key aspects integration host microbial omics-based be used comprehensive outline complex crop–microbe We describe these technological advances have helped unravel crucial genes pathways that control beneficial, pathogenic, commensal identify knowledge gaps synthesize current limitations approaches. studies which multi-omics-based approaches led improved models community structure function. Finally, recommend holistic integrating achieve precision efficiency data analysis, for biotic abiotic stress contribution microbiota shaping fitness.

Language: Английский

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Data-driven prediction of colonization outcomes for complex microbial communities

Nature Communications, Journal Year: 2024, Volume and Issue: 15(1)

Published: March 16, 2024

Microbial interactions can lead to different colonization outcomes of exogenous species, be they pathogenic or beneficial in nature. Predicting the species complex communities remains a fundamental challenge microbial ecology, mainly due our limited knowledge diverse mechanisms governing dynamics. Here, we propose data-driven approach independent any dynamics model predict from baseline compositions communities. We systematically validate this using synthetic data, finding that machine learning models not only binary outcome but also post-invasion steady-state abundance invading species. Then conduct experiments for commensal gut bacteria Enterococcus faecium and Akkermansia muciniphila hundreds human stool-derived vitro communities, confirming approaches experiments. Furthermore, find while most resident are predicted have weak negative impact on strongly interacting could significantly alter outcomes, e.g., faecalis inhibits invasion E. invasion. The presented results suggest powerful tools inform ecology management

Language: Английский

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Root exudates and microbial metabolites: signals and nutrients in plant-microbe interactions

Science China Life Sciences, Journal Year: 2025, Volume and Issue: unknown

Published: March 11, 2025

Language: Английский

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MetaFlowTrain: a highly parallelized and modular fluidic system for studying exometabolite-mediated inter-organismal interactions

Nature Communications, Journal Year: 2025, Volume and Issue: 16(1)

Published: April 10, 2025

Language: Английский

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Genome-resolved metatranscriptomics reveals conserved root colonization determinants in a synthetic microbiota

Nature Communications, Journal Year: 2023, Volume and Issue: 14(1)

Published: Dec. 13, 2023

Abstract The identification of processes activated by specific microbes during microbiota colonization plant roots has been hampered technical constraints in metatranscriptomics. These include lack reference genomes, high representation host or microbial rRNA sequences datasets, difficulty to experimentally validate gene functions. Here, we recolonized germ-free Arabidopsis thaliana with a synthetic, yet representative root comprising 106 genome-sequenced bacterial and fungal isolates. We used multi-kingdom depletion, deep RNA-sequencing read mapping against genomes analyse the planta metatranscriptome abundant colonizers. identified over 3,000 genes that were differentially regulated at soil-root interface. Translation energy production consistently planta, their induction correlated strains’ abundance roots. Finally, targeted mutagenesis show several induced multiple bacteria are required for one strains (a genetically tractable Rhodanobacter ). Our results indicate members activate strain-specific but also common sets colonize

Language: Английский

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