There is a silent conversation going on under your feet; plant roots are communicating with soil fungi through a language of small molecules. Until now, the complex genetics of these fungi made it difficult to study how they perceive small molecules directly.

The Lumba lab and the McCourt lab at the University of Toronto have published research that begins the translation of this secret language in Molecular Cell. They cracked the code by beginning with the model fungus, baker’s yeast. Baker’s yeast is a fungus domesticated by humans for millennia, and their genetic tractability make them well suited to experimentation.

They used strigolactone molecules, which are released into the soil when plants are starving for phosphate nutrients. These chemicals attract certain fungi, which grow within plant roots and transfer phosphate to the plant, leading to improved growth.

Lumba’s lab treated yeast with strigolactone and determined which genes changed in expression. The exciting results made them jump up and pull the rest of the team to the computer to see their finding: the list of most activated genes was dominated by gene labelled “PHO”! The PHO label reflects the gene’s role in response to phosphate starvation. Given that strigolactones are made by plants to coax fungi into providing phosphate for the plant, this was very intriguing.

To probe this response further, James Bradley and co-author Michael Bunsick conducted exhaustive genetic screens revealing that a high-affinity phosphate transporter in the plasma membrane, Pho84, was potentially targeted by strigolactones.

Working with Dario Bonetta at Ontario Tech, they showed that strigolactones could bind Pho84 and that they inhibited phosphate uptake. They also observed that strigolactone treatment caused the Pho84 to be taken away from the cell surface, preventing this transporter from bringing phosphate into the cell.

A combination of mutant analysis and in silico docking conducted by co-author George Ly defined a binding pocket in the Pho84 protein. As would be expected for a binding pocket, changes in the amino acid sequence in this region rendered yeast strigolactone-insensitive.

So, the Lumba lab has teased out a single phrase in the secret language of the soil, but does this phrase mean anything to wild fungus, or do domesticated yeast speak a different dialect? There are two wild fungal species, Fusarium graminearum and Serendipita indica, that were studied in this paper. F. graminearum is a blight on wheat crops in Canada, whereas S. indica promotes plant growth through symbiosis.

The results show that both F. graminearum and S. indica respond to strigolactone by altering phosphate metabolism, showing that strigolactone’s effects are conserved in wild fungi.

Dr. Gopal Subramaniam collaborated with the Lumba lab to conduct pioneering gene editing experiments on F. graminearum. They were excited to find that the F. graminearum’s response to strigolactone acts through the Pho84 transporter.

Scientists can therefore use an approach centered around baker’s yeast to systematically identify and decipher plant-derived small molecules that communicate with fungi.

As we begin to understand this secret language of small molecules, we will understand how the diversity of roots, fungi and bacteria is maintained in the soil ecosystem. This will lead to healthier crops and improve our approach to biodiversity.

You can read more about these results in “Modulation of fungal phosphate homeostasis by the plant hormone strigolactone” from Molecular Cell