Crying out for help with root exudates: adaptive mechanisms by which stressed plants assemble health-promoting soil microbiomes

Rolfe, Stephen A.; Griffiths, Joseph; Ton, Jurriaan

doi:10.1016/j.mib.2019.10.003

Cited by 322 publications

(228 citation statements)

References 80 publications

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“…This is noteworthy, as rhizosphere communities are much more diverse than internalized plant communities, and rhizosphere dynamics can have profound impacts on plant fitness (reviewed by [1,69]). Microbes are recruited to the rhizosphere by plant exudate production (reviewed by [70]). These exudates can provide a nutrient source and interact with edaphic conditions to generate a distinct environment from the surrounding soil that facilitates microbial growth, setting the stage for myriad microbe-microbe interactions that shape this dynamic community [1,71].…”

Section: Soil Origin Influences the Microbiomementioning

confidence: 99%

Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula

et al. 2020

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Background Understanding the genetic and environmental factors that structure plant microbiomes is necessary for leveraging these interactions to address critical needs in agriculture, conservation, and sustainability. Legumes, which form root nodule symbioses with nitrogen-fixing rhizobia, have served as model plants for understanding the genetics and evolution of beneficial plant-microbe interactions for decades, and thus have added value as models of plant-microbiome interactions. Here we use a common garden experiment with 16S rRNA gene amplicon and shotgun metagenomic sequencing to study the drivers of microbiome diversity and composition in three genotypes of the model legume Medicago truncatula grown in two native soil communities. Results Bacterial diversity decreased between external (rhizosphere) and internal plant compartments (root endosphere, nodule endosphere, and leaf endosphere). Community composition was shaped by strong compartment × soil origin and compartment × plant genotype interactions, driven by significant soil origin effects in the rhizosphere and significant plant genotype effects in the root endosphere. Nevertheless, all compartments were dominated by Ensifer, the genus of rhizobia that forms root nodule symbiosis with M. truncatula, and additional shotgun metagenomic sequencing suggests that the nodulating Ensifer were not genetically distinguishable from those elsewhere in the plant. We also identify a handful of OTUs that are common in nodule tissues, which are likely colonized from the root endosphere. Conclusions Our results demonstrate strong host filtering effects, with rhizospheres driven by soil origin and internal plant compartments driven by host genetics, and identify several key nodule-inhabiting taxa that coexist with rhizobia in the native range. Our results set the stage for future functional genetic experiments aimed at expanding our pairwise understanding of legume-rhizobium symbiosis toward a more mechanistic understanding of plant microbiomes.

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Section: Soil Origin Influences the Microbiomementioning

confidence: 99%

Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula

et al. 2020

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“…Likewise, this scenario is compatible with a limited number of genes controlling the biosynthesis and rhizodeposition of defensive secondary metabolites which have been implicated in shaping the plant microbiota 44 . Among these compounds, the indol-alkaloids benzoxazinoids recently gained centre-stage as master regulators of the maize-associated microbial communities 45–47 .…”

Section: Discussionmentioning

confidence: 84%

A footprint of plant eco-geographic adaptation on the composition of the barley rhizosphere bacterial microbiota

Terrazas

Balbirnie-Cumming

Morris

et al. 2020

Preprint

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The microbiota thriving in the rhizosphere, the thin layer of soil surrounding plant roots, plays a critical role in plant’s adaptation to the environment. Domestication and breeding selection have progressively differentiated the microbiota of modern crops from the ones of their wild ancestors. However, the impact of eco-geographical constraints faced by domesticated plants and crop wild relatives on recruitment and maintenance of the rhizosphere microbiota remains to be fully elucidated. Here we performed a comparative 16S rRNA gene survey of the rhizosphere of 4 domesticated and 20 wild barley (Hordeum vulgare) genotypes grown in an agricultural soil under controlled environmental conditions. We demonstrated the enrichment of individual bacteria mirrored the distinct eco-geographical constraints faced by their host plants. Unexpectedly, Elite varieties exerted a stronger genotype effect on the rhizosphere microbiota when compared with wild barley genotypes adapted to desert environments with a preferential enrichment for members of Actinobacteria. Finally, in wild barley genotypes, we discovered a limited, but significant, correlation between microbiota diversity and host genomic diversity. Our results revealed a footprint of the host’s adaptation to the environment on the assembly of the bacteria thriving at the root-soil interface. In the tested conditions, this recruitment cue layered atop of the distinct evolutionary trajectories of wild and domesticated plants and, at least in part, is encoded by the barley genome. This knowledge will be critical to design experimental approaches aimed at elucidating the recruitment cues of the barley microbiota across a range of soil types.

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“…vegetative, bolting). In support of this hypothesis, root exudates can promote the activity of symbiotic microbes, such as phosphate solubilizing bacteria and siderophore-releasing bacteria and exert mobilization of non-available plant nutrients in soils at a single growth stage [62][63][64].…”

Section: Discussionmentioning

confidence: 92%

Role of root exudates on assimilation of phosphorus in young and old Arabidopsis thaliana plants

Pantigoso

Yuan

et al. 2020

PLoS ONE

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The role of root exudates has long been recognized for its potential to improve nutrient use efficiency in cropping systems. However, studies addressing the variability of root exudates involved in phosphorus solubilization across plant developmental stages remain scarce. Here, we grew Arabidopsis thaliana seedlings in sterile liquid culture with a low, medium, or high concentration of phosphate and measured the composition of the root exudate at seedling, vegetative, and bolting stages. The exudates changed in response to the incremental addition of phosphorus, starting from the vegetative stage. Specific metabolites decreased in relation to phosphate concentration supplementation at specific stages of development. Some of those metabolites were tested for their phosphate solubilizing activity, and 3-hydroxypropionic acid, malic acid, and nicotinic acid were able to solubilize calcium phosphate from both solid and liquid media. In summary, our data suggest that plants can release distinct compounds to deal with phosphorus deficiency needs influenced by the phosphorus nutritional status at varying developmental stages.

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Crying out for help with root exudates: adaptive mechanisms by which stressed plants assemble health-promoting soil microbiomes

Cited by 322 publications

References 80 publications

Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula

Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula

A footprint of plant eco-geographic adaptation on the composition of the barley rhizosphere bacterial microbiota

Role of root exudates on assimilation of phosphorus in young and old Arabidopsis thaliana plants

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