Boyce Thompson Institute scientists discover new structures at the plant-fungal interface

A new discovery could potentially help reduce fertilizer use in agriculture

For hundreds of millions of years, plants and fungi have formed symbiotic relationships to exchange essential nutrients, such as phosphate and fatty acids. This relationship is extremely important for the growth and survival of both organisms, and solving the mystery of how they transfer molecules to each other could eventually help reduce fertilizer use in agriculture.

Today, researchers at the Boyce Thompson Institute (BTI) have discovered structural tubule networks at the plant-fungal interface that could shed light on the mechanisms of this natural partnership. Details of the study were published in Nature Plants on February 8.

It is estimated that 80% of vascular plant families form symbioses with a type of soil fungus called arbuscular mycorrhizal fungi. Fungi penetrate the outermost cells of a plant's roots and develop complex branch-shaped structures called arbuscles. Each host plant cell then grows a membrane that envelops a shrub, and the exchange of nutrients takes place in the space between the plant membrane and the fungal cell wall.

In an attempt to understand the fundamental interaction between plants and fungi, Maria Harrison, a BTI faculty member, and Sergey Ivanov, a postdoctoral fellow, joined R. Howard Berg, Director of the Donald Danforth Centre for Integrated Microscopy. They used advanced electron microscopy techniques to visualize the arbuscles present in the roots of the legume Medicago truncatula colonized by the fungus Rhizophagus irregularis, and were surprised by the results.

"Our understanding of the subcellular structural basis of interaction is based on studies conducted 30 to 40 years ago. Many of them indicated that the material around the fungus but inside the plant membrane would be an amorphous matrix of carbohydrate material," said Harrison, the corresponding author of the article. Instead, the researchers found a network of round, tubular and dumbbell-shaped structures made up of lipid membranes, almost all of which appeared to connect to the membrane of the plant cell.

The researchers were also surprised to find another network of membrane tubules in the space between the fungal cell membrane and the fungal cell wall. "It was quite unexpected to see such a large proliferation of the fungal membrane, especially when you know that the fungus is hungry for lipids," explains Ivanov, the lead author of the article.

Harrison and Ivanov speculate that networks are linked to lipid transfer.

"Somehow, lipids are released by the plant cells and fed to the fungus, and we wondered how they move through what we thought was an aqueous matrix between the plant cell membrane and the fungal cell wall," says Harrison. "But maybe this space is not so aqueous after all, and maybe this membrane-rich environment facilitates the movement of lipids between organisms."

Given the physical proximity between plant and fungal membrane networks, the fungal network could be involved in lipid absorption to optimize the process. The researchers suspect that the network is not involved in the transfer of phosphate to the plant because membrane networks are more abundant near the large branches of the shrub, while phosphate absorption probably occurs near the small branches.

Harrison believes that new technologies are to be thanked for finding these tubule networks. "The fixation of samples by high-pressure freezing allows a better preservation of the membrane than older techniques. I think that's why these extended membranes have never been seen before," she says. "In addition, 3D electron tomography is very powerful and allows to visualize networks, which did not seem connected to 2D images."

Ivanov worked closely with Berg, an expert in cryofixation and electron microscopy, and Jotham Austin II of the University of Chicago, an expert in tomography. Financial support for this project was provided by the United States National Science Foundation Grant No. IOS-1353367 and the TRIAD Foundation.

Another research group led by Uta Paszkowski from the University of Cambridge in the United Kingdom has carried out similar imaging studies on rice colonized by R. irregularis and found similar structures. These results were published in the same issue of Nature Plants.