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 Genes that control root endodermal function in the model plant Arabidopsis thaliana contribute to the plant root microbiome assembly. 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. 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.

中文翻译：

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微生物群和根内皮层之间的协调支持植物矿物质营养稳态

微生物改变植物根系渗透性根系为植物提供矿物质养分和水分。扩散屏障密封根部，防止内部水分和养分流失。萨拉斯-冈萨雷斯等人。发现生活在模式植物拟南芥根部和根部的微生物会影响扩散屏障的形成，从而影响植物中矿质养分的平衡（参见 Busch 和 Chory 的观点）。具有改良根扩散屏障的植物显示出改变的细菌群落组成。微生物利用植物的脱落酸激素信号来稳定根扩散屏障，防止环境养分可用性受到干扰，从而增强植物的抗逆性。科学，这个问题 p。eabd0695; 另见第 在模式植物拟南芥中控制根内胚层功能的 125 个基因有助于植物根微生物组的组装。引言 所有生物体都进化出稳态机制来控制它们的矿物质营养和微量元素含量（离子体）。在植物根部和动物肠道中，这些机制涉及专门的细胞层，这些细胞层充当水、溶质和免疫活性配体的扩散屏障。为了发挥这一作用，形成这些层的细胞必须紧密密封在一起。此外，这些细胞必须在与局部微生物群相互作用的同时执行其稳态功能。在动物中，常驻微生物会影响肠道扩散屏障的功能，在某些情况下，这种相互作用的失调会导致生态失调。在植物中，在内皮层有两种类型的细胞外根扩散屏障的特征：将细胞密封在一起的 Casparian 条带和影响跨细胞质膜运输的木栓质沉积物。这些根系扩散障碍是否以及如何与栖息在根部的微生物群协调尚不清楚。这种协调可能会影响植物性能、农艺产量和作物的营养质量。基本原理我们探索并表征了控制根扩散屏障性能的调节网络与栖息在根中的功能复杂且代谢动态的微生物群之间的相互作用。为了解决这个问题，我们使用两种互补的方法探索了这种交互的推定互惠性质。第一的，我们对一组植物的微生物组进行了分析，这些植物对根扩散屏障进行了一系列特定的改变，以确定控制屏障组分合成和沉积的调节网络是否也控制了根微生物组的结构。其次，我们部署了一系列从天然土壤中生长的植物的芽和根中分离出来的细菌菌株，以确定微生物组对根屏障功能的影响。最后，我们将两种方法结合起来，以确定根扩散屏障与其相关微生物群之间的分子联系。结果我们分析了 19 个根扩散屏障突变体和过表达系的非冗余和多样化集合，以揭示根扩散屏障调节网络对植物微生物群组装的影响。我们筛选了 416 个单独的细菌菌株，因为它们能够改变内皮层中的 Casparian 带和木栓质沉积物的功能，并发现植物微生物群在影响根扩散屏障功能以及影响植物矿物质营养稳态方面的新作用。我们设计并部署了一个结合离子组学和转录组学的细菌合成群落，以发现根系扩散障碍与植物微生物群之间协调的分子机制。我们的研究有三个主要发现：(i) 控制内胚层根扩散障碍的调节网络也影响植物微生物群的组成；(ii) 植物微生物组、细菌合成群落的个体成员，或天然微生物群落控制内胚层扩散障碍的发展，尤其是木栓质沉积，对植物的离体和非生物胁迫耐受性产生影响；(iii) 植物微生物群影响根扩散屏障功能的能力是通过抑制依赖于植物激素脱落酸的信号传导来介导的。结论我们关于植物微生物群影响根扩散屏障功能的发现概括了微生物群在控制跨界细胞扩散屏障中的作用。此外，我们定义了多细胞生物中的扩散屏障如何结合微生物功能来调节矿物质营养平衡的分子基础。这一发现在植物和人类营养以及食品质量和安全方面具有潜在的应用价值。基于微生物的控制植物根系松软化的策略为设计更具弹性的作物、新的生物强化策略和碳封存方法提供了新的机会。微生物群影响根系扩散障碍。(A) 模型显示微生物群和根扩散障碍之间的相互作用。微生物影响 Casparian 条带的合成，并选择基于植物的脱落酸信号来控制内胚层松解。(B) 在无菌条件下或根系微生物群中生长的植物中木栓质积累的示意图。根系微生物减少内胚层松解，优化植物中的矿物质营养稳态和非生物胁迫反应。植物根和动物内脏已经进化出专门的细胞层来控制矿物质营养稳态。这些层必须容忍常驻微生物群，同时保持稳态完整性。内胚层中的根扩散屏障对植物的矿物质营养平衡至关重要，是否以及如何与微生物群协调尚不清楚。我们证明了在模式植物拟南芥中控制内胚层功能的基因有助于植物微生物组的组装。我们描述了一种由微生物群驱动的内胚层分化调节机制，对营养稳态产生深远的影响。此外，我们证明这种机制与微生物群抑制对根中植物激素脱落酸反应的能力有关。我们的研究结果将内皮层确立为协调微生物群组装和稳态机制的调节中心。