Plant-bacteria partnership reveals how roots access iron locked in soil

A new study led by Paul Schulze-Lefert from the Max Planck Institute for Plant Breeding Research in Cologne, in collaboration with Ricardo F.H. Giehl at the Leibniz Institute of Plant Genetics and Crop Plant Research in Gatersleben, revealed how Arabidopsis plants adapt their chemical communication with the bacterial root microbiota to maximize the acquisition of bio-unavailable iron from acidic or calcareous soils. The study is now published in Cell.

Iron is essential for plant growth, yet in many soils it remains out of reach for plants. The reason is chemical: much of the iron is locked in insoluble forms that roots cannot directly absorb. As a result, plants have evolved strategies to unlock and acquire this essential micronutrient from soils. These hidden mechanisms are crucial for healthy plant growth and, ultimately, for the productivity of the crops that sustain global food systems.

All healthy plants grown in natural soils are colonized by a diverse community of microbes, known as the microbiota. To cope with iron limitation, plants such as Arabidopsis thaliana and many crop species activate a sophisticated iron starvation response. This starvation response involves the release of specialized molecules, often coumarins, from the roots into the rhizosphere—the narrow zone of soil surrounding the plant roots and inhabited by the root microbiota.

Coumarins come in different “flavors.” Arabidopsis adjusts the release of different coumarin chemotypes according to soil pH: sideretin is the main coumarin secreted by roots in acidic soils, while more fraxetin is released in calcareous soils. These chemicals can mobilize bio-unavailable iron and are thought to be an adaptation to soil pH to maximize iron acquisition. Yet paradoxically, plants grown without their bacterial root microbiota remain iron-deficient.

Previous studies have shown that root-associated bacteria can help plants overcome iron deficiency, with fraxetin playing a key role in calcareous soils at near-neutral pH. However, it remained unclear whether root-associated bacteria support pH-adaptive iron acquisition—together with the different coumarins released—and how these coumarins interact with the bacteria.

Chemical communication with the little helpers results in synergy

Using genetic and chemical approaches in plants and bacteria, the team found that sideretin and fraxetin interact with a wide range of root-associated bacteria and help mobilize iron in the soil, making it more accessible to the plant. Importantly, while the pH-adapted release of these coumarins by the plant occurs in the absence of microbes, their full function in iron mobilization is only seen in synergy with the root microbiota.

Further analyses revealed two mechanisms for iron mobilization by which the bacteria interact with these pH-specific coumarins.

At an acidic pH, trivalent iron (Fe(III)), which is a dominant, bio-unavailable form in soil, is reduced to the more soluble divalent form (Fe(II)) through a process called reductive dissolution. This leaves behind an inactive, oxidized form of sideretin. Bacteria interact with sideretin through a bacterial redox-sensing mechanism. Through this mechanism, used-up sideretin is proposed to be imported by the bacteria for recycling and subsequent release into the rhizosphere to reduce more iron (Fe(III)). This process is called a bacterial redox shuttle.

In contrast, at near-neutral pH, the interactive mobilization of Fe(III) takes place through an interaction between the coumarin fraxetin and a bacterial siderophore. Siderophores are molecules produced and released by the bacteria for their own iron acquisition when a shortage is detected. Fraxetin apparently diverts some of the siderophore-mobilized iron for plant iron acquisition.

These two bacterial traits are widespread in the root microbiota. This suggests that these bacterial processes likely evolved long before land plants emerged. They are known to play an important role in how bacteria adapt to changing environmental conditions in soils. Hence, plants utilize these ancient microbial traits via secreted coumarins to mobilize iron and overcome nutritional iron deficiency.

Most of the tested root-associated bacteria were able to rescue plants from iron deficiency when co-cultured under different pH conditions in the laboratory. This was true regardless of whether the bacteria were collected from plants grown in iron-sufficient or iron-deficient soil. This suggests that the capacity of bacteria to mobilize iron at different pH levels is prevalent across different soils. Thus, these two bacterial mechanisms can be activated flexibly by the plant on demand through the release of different coumarins in response to soil pH.

Overall, this indicates that the pH-dependent release of different coumarin chemotypes is an adaptive trait that enables plants to acquire iron in a microbial environment with varying soil pH.

The plant also calls little helpers to acquire phosphate

In a recent study from an international team including Schulze-Lefert from the MPIPZ, Arabidopsis plants were shown to cooperate with root-associated bacteria to mobilize the macronutrient phosphorus from soil. As with iron, most of the phosphorus in soil is locked away in forms that are unavailable to plants.

When phosphorus is scarce, Arabidopsis roots in this case release malate. Rather than extracting significant amounts of phosphorus directly, malate acts as a “call-for-help” signal that attracts phosphorus-solubilizing bacteria to the root surface.

Once there, the bacteria adopt a new lifestyle. They consume carbon and nitrogen compounds supplied by the plant host and activate mechanisms that release phosphorus from otherwise inaccessible inorganic and organic sources. The phosphorus then supports the growth of both the bacteria and the plant.

Application for sustainable agriculture

Even though different mechanisms are in place for overcoming iron or phosphorus limitations, specific molecules are released by the plant that cause the surrounding microbes to support plant growth.

This fundamental knowledge is important for the future development of rationally designed biofertilizer microbes or biomimetic molecules that can reduce the use of synthetic fertilizers in agricultural production systems.

“Plants have never existed without microbes, and many of their traits likely reflect this shared history. Uncovering the molecular basis of these beneficial interactions with microbes will create new opportunities for sustainable agriculture,” says Milena Malisic.

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