Abstract
Plant roots and animal guts have evolved specialized cell layers to control mineral nutrient homeostasis. These layers must tolerate the resident microbiota while keeping homeostatic integrity. Whether and how the root diffusion barriers in the endodermis, which are critical for the mineral nutrient balance of plants, coordinate with the microbiota is unknown. We demonstrate that genes controlling endodermal function in the model plant Arabidopsis thaliana contribute to the plant microbiome assembly. We characterized a regulatory mechanism of endodermal differentiation driven by the microbiota with profound effects on nutrient homeostasis. Furthermore, we demonstrate that this mechanism is linked to the microbiota's capacity to repress responses to the phytohormone abscisic acid in the root. Our findings establish the endodermis as a regulatory hub coordinating microbiota assembly and homeostatic mechanisms.
Highlights
Expected from a plant-derived mechanism, we consistently observed these differences in root and shoot, but not in the soil fraction (Fig. 1A, S1E, and S1F)
These results indicate that Casparian strip synthesis is more resilient to the effect of individual bacteria than endodermal suberization, and that members of the plant microbiome can modify suberin deposition independently of the Casparian strip. 124 we used the representative subset (n=41) of the bacterial strains in plant-association assays to test whether their effect on suberization regulates plant mineral nutrient homeostasis (Fig. 2B, S6A, and S6B)
These results indicate that strains from the plant microbiome can modify suberin accumulation in the endodermis over a wide range. 138 We asked if the bacterially-induced changes in the root diffusion barriers function affect plant 139 mineral nutrient homeostasis
Summary
We demonstrate that the genes regulating root diffusion barriers influence the composition of the plant microbiota, and reciprocally that microbes colonizing the root influence root diffusion barrier function. Our findings define a mechanism allowing plants to cope with fluctuations in mineral nutrient supply in nature, and generalize the role of the microbiome in controlling diffusion barrier functions across kingdoms. Our findings improve our understanding of how diffusion barriers in multicellular organisms integrate microbial function to maintain mineral nutrient homeostasis (Fig. 4D). We anticipate the opening of unexplored avenues leading to the development of plants more adapted to extreme environmental conditions, with more capacity for carbon sequestration, high content of beneficial mineral nutrients and less toxic elements.
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