The vast majority of terrestrial plants maintain close and complex ties at root level with microscopic soil fungi. Among these ties, mycorrhizal symbiosis occurs in nearly 80% of plants – crop plants for the most part. This symbiosis gives plants better access to minerals in the soil, including phosphorus. As they evolved, plants of Brassicaceae family, such as Arabidopsis thaliana, or thale cress, lost their ability to establish mycorrhizal associations and the resulting nutritional benefits. Against all odds, researchers at INRA Versailles-Grignon, with their German, Spanish and Japanese colleagues, discovered the asymptomatic presence of the microscopic fungus Colletotrichum tofieldiae in certain naturally-occurring populations of A. thaliana. They quickly explored this original discovery to understand its potential.
An association that begins at root level
The scientists showed that Colletotrichum tofieldiae initially colonises roots, entering and passing between plant cells. The fungus then spreads to the plant’s growing shoots, showing the clear endophytic nature of the fungus. C. tofieldiae causes no visible symptoms in A. thaliana, despite belonging to one of the biggest groups of fungal plant pathogens in the world.
Cooperation with benefits
By observing the impact of colonisation of the host plant, the scientists discovered that the presence of C. tofieldiae increases growth and fertility in A. thaliana in phosphate-poor conditions. This improvement is due to the conversion by the fungus of insoluble phosphate into soluble phosphate. The mineral is then carried from the fungal cells to the host plant cells, where it can then be used. This transfer of phosphate to the plant cells is activated by the fungus favoured by an increase in the expression of several specialised plant transmitters.
How does the plant control this interaction? It uses a phosphate starvation response (PSR) system which allows it to measure the availability of phosphate in the soil. The scientists showed that this PSR system is essential to plant growth promotion (PGP) via the fungus and to controlling the fungus’s colonisation of the plant. The plant also uses a component of its immune system involved in the synthesis of glucosinolates, a type of antimicrobial compound. Without these molecules, C. tofieldiae becomes a formidable pathogen for A. thaliana.
This work once again highlights the role played by a plant’s immune system in establishing a beneficial association with a fungus which ensures a nutrient supply in nutrient-poor conditions. The research demonstrates that the extent to which the association is beneficial to the plant is determined by environmental factors and particularly by the amount of phosphate to which the plant has access. By offering a new example of interaction between plants and soil fungi, this research suggests that in phosphate-deprived soils, plant root colonisation by C. tofieldiae compensates for a lack of traditional mycorrhizal associations in plants of the Brassicaceae family.
Hiruma K, Gerlach N, Sacristán N, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell RJ, Schulze-Lefert P (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status-dependent.Cell 165: 1. http://dx.doi.org/10.1016/j.cell.2016.02.028