Research Article

Coordination between microbiota and root endodermis supports plant mineral nutrient homeostasis

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Science  08 Jan 2021:
Vol. 371, Issue 6525, eabd0695
DOI: 10.1126/science.abd0695

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Microbes modify plant root permeability

The root provides mineral nutrients and water to the plant. Diffusion barriers seal the root, preventing the loss of internal water and nutrients. Salas-González et al. found that microbes living on and in roots of the model plant Arabidopsis thaliana influence diffusion barrier formation, which affects the balance of mineral nutrients in the plant (see the Perspective by Busch and Chory). Plants with modified root diffusion barriers show altered bacterial community composition. Microbes tap into the plant's abscisic acid hormone signals to stabilize the root diffusion barrier against perturbations in environmental nutrient availability, thus enhancing plant stress tolerance.

Science, this issue p. eabd0695; see also p. 125

Structured Abstract

INTRODUCTION

All living organisms have evolved homeostatic mechanisms to control their mineral nutrient and trace element content (ionomes). In plant roots and animal guts, these mechanisms involve specialized cell layers that function as a diffusion barrier to water, solutes, and immunoactive ligands. To perform this role, it is essential that the cells forming these layers are tightly sealed together. Additionally, these cells must perform their homeostatic function while interacting with the local microbiota. In animals, resident microbes influence the function of intestinal diffusion barriers and, in some cases, miscoordination of this interplay can cause dysbiosis.

In plants, two types of extracellular root diffusion barriers have been characterized at the endodermis: Casparian strips, which seal cells together, and suberin deposits, which influence transport across the cell plasma membrane. Whether and how these root diffusion barriers coordinate with the microbiota inhabiting the root is unknown. Such coordination could influence plant performance, agronomic yields, and the nutritional quality of crops.

RATIONALE

We explored and characterized the interplay between the regulatory networks controlling the performance of the root diffusion barrier and the functionally complex and metabolically dynamic microbiota inhabiting the root. To address this, we explored the presumptive reciprocal nature of this interaction using two complementary approaches.

First, we profiled the microbiome of a collection of plants with a range of specific alterations to the root diffusion barrier to determine whether the regulatory network controlling the synthesis and deposition of the barrier components also controls the structure of the root microbiome. Second, we deployed a collection of bacterial strains isolated from the shoots and roots of plants grown in natural soils to establish the influence of the microbiome over root barrier function. Last, we coupled both approaches to identify the molecular links between the root diffusion barrier and their associated microbiota.

RESULTS

We analyzed a nonredundant and diverse collection of 19 root diffusion barrier mutants and overexpression lines to reveal the influence of the root diffusion barrier regulatory network on the assembly of the plant microbiota. We screened 416 individual bacterial strains for their ability to modify the function of the Casparian strip and suberin deposits in the endodermis and uncovered a new role for the plant microbiota in influencing root diffusion barrier functions with an impact on plant mineral nutrient homeostasis. We designed and deployed a bacterial synthetic community combined with ionomics and transcriptomics to discover the molecular mechanisms underlying the coordination between root diffusion barriers and the plant microbiota.

Our research has three main findings: (i) The regulatory network controlling the endodermal root diffusion barriers also influences the composition of the plant microbiota; (ii) individual members of the plant microbiome, bacterial synthetic communities, or natural microbial communities control the development of endodermal diffusion barriers, especially suberin deposition, with consequences for the plant’s ionome and abiotic stress tolerance; and (iii) the capacity of the plant microbiome to influence root diffusion barrier function is mediated by its suppression of signaling dependent on the phytohormone abscisic acid.

CONCLUSION

Our findings that the plant microbiome influences root diffusion barrier function generalizes the role of the microbiome in controlling cellular diffusion barriers across kingdoms. In addition, we defined the molecular basis of how diffusion barriers in multicellular organisms incorporate microbial function to regulate mineral nutrient balance. This discovery has potential applications in plant and human nutrition and food quality and safety. Microbial-based strategies to control suberization of plant roots presents new opportunities to design more resilient crops, new biofortification strategies, and carbon-sequestration approaches.

The microbiota influences root diffusion barriers.

(A) Model showing the interplay between the microbiota and root diffusion barriers. Microbes influence Casparian strip synthesis and co-opt plant-based abscisic acid signaling to control endodermal suberization. (B) Schematic representation of suberin accumulation in plants grown under axenic conditions or with the root microbiota. Root-inhabiting microbes reduce endodermal suberization optimizing mineral nutrient homeostasis and abiotic stress responses in the plant.

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.

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