Plants and animals rely on iron for growth and regulation of microbiomes, the collections of microorganisms that co-exist in places such as the human gut, and the soil around a plant’s roots. Plants face a special challenge when acquiring iron, since the strategies they use to increase iron availability alter the root microbiome and can inadvertently benefit harmful soil-dwelling bacteria.

Salk Institute scientists have now found that plants can manage iron deficiency without helping “bad” bacteria thrive, by eliminating IMA1 (Iron Man 1), the molecular signal for iron deficiency in roots at risk of bacterial attack. The team’s studies also discovered that more IMA1 in leaves can make them more resistant to bacterial attack, suggesting the iron deficiency signaling pathway and plant immune system are deeply intertwined. The results could offer up a new potential target to help improve plant resilience.

“Microbes determine the fate of carbon in soil, so uncovering how plants react to and impact their soil microenvironment can teach us a lot about optimizing plant carbon storage,” said Wolfgang Busch, PhD, executive director of Salk’s Harnessing Plants Initiative “Relatedly, understanding how plants regulate signaling and immune responses in the face of environmental scarcities, like iron deficiencies, will be crucial as scientists optimize plant health in our continually changing climate.”

Busch is senior author of the team’s published paper in Nature, which is titled “Spatial IMA1 regulation restricts root iron acquisition on MAMP perception.”

Iron is an essential nutrient for growth among all branches of life, the authors wrote, but while iron is among the most common elements on the plant, bioavailable iron—iron in a state that plants and animals can use—is a relatively scarce nutrient. “Consequently, strong competition for iron is common between organisms.”  Among plants iron deficiency—and consequential stunted plant growth—is not uncommon. Since stopping growth is not ideal, plants have developed techniques to encourage iron absorption in low-iron environments. Unfortunately, those techniques can also alter the entire microbiome around the roots and increase iron availability for not just the plant, but for the harmful bacteria living nearby, too.

“Overall, iron has an important but complex role in regulating plant–microorganism interactions,” the team continued. “However, much about this multifaced interaction that includes plants, beneficial or commensal and pathogenic microorganisms in the rhizosphere remains to be learned.”

Plant root cross-section showing iron deficiency signal IMA1 expression (yellow) during iron deficiency (left) and iron deficiency plus simulated bacterial presence (right).
Plant root cross-section showing iron deficiency signal IMA1 expression (yellow) during iron deficiency (left) and iron deficiency plus simulated bacterial presence (right). [Salk Institute]

To help unravel the complex relationship between plant health, iron levels, and bacterial threat ,Busch and colleagues turned to the small plant model organism Arabidopsis thaliana. They grew the plant in low-iron (-Fe) and high-iron (+Fe) growth substrate, with and without flg22, a peptide fragment of bacterial flagella that would mimic the presence of bacteria.

From left: Min Cao and Wolfgang Busch. [Salk Institute]
From left: Min Cao and Wolfgang Busch. [Salk Institute]

“We hypothesized there would be some sort of competition between the plant and bacteria over the iron,” said first author Min Cao, PhD, a postdoctoral researcher in Busch’s lab. “But we found that when plants feel threatened by harmful bacteria, they are willing to stop acquiring iron and stop growing—they’ll deprive themselves in order to deprive the enemy.”

The results showed that when roots were exposed to flagella in low-iron environments, the plants mounted an unexpected response. Rather than the expected battle over iron between plant and bacteria, the plant immediately forfeited by eliminating the iron-deficiency signal IMA1. “IMA1 is a phloem mobile signal that is triggered in response to iron deficiency,” they explained. In contrast, when roots were exposed to flagella in high-iron environments, IMA1 was not eliminated, but did not need to be expressed since iron levels were sufficient.

In plants that eliminated IMA1 in response to low iron and flagella, the researchers encountered another surprise. They found that the more IMA1, the more resistant plant leaves were to bacterial attack. This observation led to the conclusion that iron availability and iron deficiency signaling help orchestrate the plant immune response. “As IMA1 is considered to be a mobile signal that relays information from the shoot to the root, we checked whether IMA1 also has a role in coordinating iron and immune responses in the shoot,” they noted. They found that IMA1 protein levels were low in the shoot under +Fe conditions, while −Fe conditions led to an accumulation of IMA1 protein in the shoot in epidermal cells, mesophyll cells and abundantly in the vascular tissue. “Treatment with flg22 under −Fe conditions decreased IMA1 protein in the epidermal cells and mesophyll cells but not in the vascular tissue, suggesting that, like in the root, there are also cell-type-specific regulatory mechanisms for IMA1 in the shoot.”

Busch, who is also the Hess Chair in Plant Science at Salk, concluded, “There is a long-established relationship between plant iron nutrition and bacteria. Exploring this relationship with more nuance allowed us to find a surprising new signaling pathway that plants use to turn off iron uptake as a defense strategy against threatening bacteria that also happens to alter the plant’s immune response.”

Plant root (gray) showing IMA1 expression (yellow) during iron deficiency (left) and iron deficiency plus simulated bacterial presence (right).
Plant root (gray) showing IMA1 expression (yellow) during iron deficiency (left) and iron deficiency plus simulated bacterial presence (right). [Salk Institute]

The authors further concluded, “Our findings reveal an adaptive molecular mechanism of nutritional immunity that affects iron bioavailability and uptake, as well as immune responses … Taken together, we propose that the antagonistic function between the IMA1-mediated iron deficiency response and the flg22-elicited defense response might be critical to avoid making iron bioavailable for potential pathogens and to avoid impairing plant defense responses.”

Busch believes IMA1 may be a useful target for optimizing plant immunity, which will become increasingly important as the planet’s climate continues to change and diseases begin to evolve more rapidly. Discovering that plants will halt iron uptake and arrest their growth in the face of potentially harmful bacteria is just one part of a more complex story that combines plant resilience, plant and animal microbiomes, and potentially climate change.

In the future, the researchers will explore whether targeting IMA1 can change plant resistance to disease, and how exactly the individual cells in plant roots shut down the IMA1 signaling pathway. Learning about plant roots can teach scientists about other absorptive tissues, like the human gut, so they can better understand the intersection of mammalian microbiomes, immune systems, and iron to optimize health.

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