Iron will: how plants deprive bacteria by depriving themselves

Plants and animals alike rely on iron for the growth and regulation of their microbiomes — but the strategies plants use to increase iron availability can inadvertently benefit harmful soil-dwelling bacteria. Scientists at the Salk Institute for Biological Studies have now discovered how plants manage iron deficiency without helping ‘bad’ bacteria thrive, with their results published in the journal Nature.

Because bioavailable iron (iron in a state that plants and animals can use) is a relatively scarce nutrient, 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 alter the entire microbiome around the roots and increase iron availability for not just the plant, but for the harmful bacteria living nearby, too.

Looking to unravel the complex relationship between plant health, iron levels and bacterial threat, Salk researchers turned to a small model plant called Arabidopsis thaliana. They grew the plant in low-iron and high-iron growth substrate (soil), then added fragments of flagella (little tails bacteria use to move) to mimic the presence of bacteria.

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 IMA1, the molecular signal for iron deficiency in roots at risk of bacterial attack. 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.

“We hypothesised there would be some sort of competition between the plant and bacteria over the iron,” said postdoctoral researcher Min Cao, first author on the study. “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.”

In plants that eliminated IMA1 in response to low iron and flagella, the researchers encountered another surprise: the more IMA1, the more resistant plant leaves were to bacterial attack. This observation led to the conclusion that iron availability and iron deficiency signalling help orchestrate the plant immune response.

Senior author Professor Wolfgang Busch believes IMA1 may be a useful target for optimising 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 thus the beginning of a much longer story about plant resilience, plant and animal microbiomes, and climate change.

“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 optimising plant carbon storage,” said Busch, who is Executive Director of Salk’s Harnessing Plants Initiative. “Relatedly, understanding how plants regulate signalling and immune responses in the face of environmental scarcities, like iron deficiencies, will be crucial as scientists optimise plant health in our continually changing climate.”

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 signalling pathway. Learning about plant roots can also 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 optimise health.

Image caption: Plant root (grey) showing IMA1 expression (yellow) during iron deficiency (left) and iron deficiency plus simulated bacterial presence (right). Image credit: Salk Institute.