Fungal Allies Shield Plant Roots, Redefine Infection

University of Cambridge

Scientists have discovered that beneficial root-dwelling fungi boost plant resilience to disease by remodelling the plant cell membrane at pathogen infection sites – offering critical new insights into how plants coordinate defences in complex natural environments.

This new research reveals that the membrane interface between plant cells and invading pathogen microbes is not fixed. Instead, it can be reshaped by co-colonising symbionts, fundamentally altering how plants interact with pathogens and potentially improving resistance to disease.

More than 80% of land plants, including many crops, form partnerships with arbuscular mycorrhizal (AM) fungi to improve nutrient uptake. These mutualistic fungi are also known to help plants resist disease, but the mechanisms behind this protective effect have remained unclear.

Researchers at the Sainsbury Laboratory Cambridge University (SLCU) have now shown that when plant roots are pre-colonised by AM fungi, the plant remodels the membrane around subsequent cell-invading pathogens.

Instead of forming the usual pathogen-associated extrahaustorial membrane (EHM), the plant produces a membrane with properties similar to the membrane surrounding AM fungi, a transition that coincides with increased disease resistance.

The work highlights that AM fungi prime root defences at a cellular and molecular level by influencing the composition and identity of these specialised membrane interfaces.

The study used Nicotiana benthamiana (a species of tobacco), which can host the beneficial AM fungus Funneliformis mosseae and later be infected by the destructive filamentous oomycete Phytophthora palmivora.

Plants form different membrane interfaces for friends and foes

When microbes (beneficial or harmful) enter living plant cells they become enclosed within a host-derived membrane that separates them from the plant cell's cytoplasm.

These membranes actively mediate nutrient exchange and molecular communication between plants and microbes, but their structure differs markedly between mutualistic and pathogenic interactions.

Mutualistic fungi form arbuscules inside roots cells encased in a periarbuscular membrane (PAM), while filamentous pathogens produce haustoria surrounded by an EHM.

Friendly fungi flip the playbook by changing the plant's cellular interface

This is the first demonstration that AM fungi can alter the EHM of a pathogen that arrives later.

Published in Cell Reports, the study co-led by Dr Alex Guyon and Professor Sebastian Schornack , shows that AM fungi can effectively overwrite the normal distinction between mutualistic and pathogenic interfaces.

"We found that the pathogen's strategy completely fell apart in the presence of the mutualist," said Dr Guyon, who conducted the research as part of his PhD. "In these co-colonised roots, the pathogen's membrane identity was rewired and now contained a new signalling lipid and membrane-tethered proteins."

This transformation coincided with a significant reduction in pathogen colonisation.

"These findings fundamentally change our view of plant immunity and symbiosis," said Professor Sebastian Schornack, who is a group leader at SLCU. "They show that the long-established symbiotic process of enforcing a specific membrane composition may overrule the pathogen's attempts to manipulate the host cell. To fully understand this molecular mechanism, we must now look beyond single-microbe systems to understand how plants coordinate defences in the face of complex microbial communities that plants encounter in nature."

Why this matters

AM fungi not only improve plant nutrition, they also strengthen plant defences against pathogens. Understanding how they enhance disease resistance opens new possibilities for using beneficial fungi as natural biocontrol agents to improve crop resilience.

This research highlights a new front in the battle between plants and pathogens, showing that AM fungi can reprogramme membrane interfaces at infection sites. These insights offer promising avenues for developing future strategies to boost crop resilience by leveraging beneficial microbes.

How the research was done

To better reflect natural conditions where plants are colonised by diverse microbial communities and even individual cells can host multiple microbes, the researchers used Nicotiana benthamiana, a species of tobacco and model research plant that can simultaneously accommodate both AM fungi and pathogenic oomycetes.

To track changes in the host's cellular membranes in real time, the team developed and characterised phospholipid reporter lines in N. benthamiana by integrating phospholipid biosensors, which were previously established in Arabidopsis thaliana by Yvon Jaillais's group at ENS Lyon .

Researchers investigated the role of phosphoinositides (PIPs), which are a class of signalling lipids that act like molecular "identity tags" on cell membranes, dictating how the cell functions.

Under controlled laboratory conditions, the team confirmed that the two microbes established distinct membrane identities.

The mutualistic AM fungus Funneliformis mosseae was surrounded by a membrane rich in PI4P.

In contrast, the pathogenic oomycete Phytophthora palmivora successfully excluded key host components, including PI4P and a myristoylated protein (usually tethered to host plasma membranes) from its EHM. This exclusion may be a pathogen-driven strategy, possibly to suppress the host's immune response.

Co-colonisation flips the script

The critical discovery came from simulating a more natural scenario where the plant roots were pre-colonised by the mutualist fungus before being attacked by the pathogen.

Strikingly, in roots pre-colonised by AM fungi, the pathogen's EHM composition was dramatically re-wired. PI4P and myristoylated proteins were now present around the pathogen's haustorium, making the EHM resemble the PAM of the mutualist.

This demonstrated that host membrane identity is not static and can be dynamically reshaped by co-colonisation, altering the properties of the pathogen's intracellular interface.

Crucially, this change in membrane identity coincided with enhanced resistance and reduced colonisation by P. palmivora.

Interestingly, neighbouring root cells, which may have recently, but not currently been colonised by AM fungi, also showed altered membrane composition at pathogen entry sites, although this effect was confined to roots and not observed in leaves.

Funding

Funding for this project was provided by the School of Biological Sciences Doctoral Training Programme, the Royal Society and The Gatsby Charitable Foundation.

Reference

Alex Guyon, Theresa Staps, Lyne Badot, Sebastian Schornack (2025) Mutualist-pathogen co-colonization modulates phosphoinositide signatures at host intracellular interfaces. Cell Reports DOI: 10.1016/j.celrep.2025.116702

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