A beneficial fungus uses glucose concentrations to balance cellulase production and to recognize living plants, which accelerate fungal development

Fungi are among the most important degraders of dead plant materials and hence fuel the global carbon cycle. Production of the enzymes required for plant cell wall degradation is tightly regulated in fungi by environmental conditions including nutrient quality and quantity, temperature, pH and light. This sophisticated regulation indicates that the energy intensive production of enzymes is optimized to fulfil the needs of the fungus but to minimize excess and avoid feeding of so-called “exploiter-“ or “cheater-“microbes.

We therefore asked how fungi sense degradable material and discriminate to root exudates or living tissue of plants to balance enzyme production with available resources. With the filamentous saprophyte Trichoderma reesei we identified two cell-surface receptors (CSG1 and CSG2), which are distinct from previously identified glucose sensors. T. reesei uses detection of a precise amount of glucose, but not other sugars released from plant materials, by these receptors as a proxy for cellulosic material to initiate translation of cellulases. Also special attachment structures formed by T. reesei on natural plant material are missing in the absence of CSG1 or CSG2. Moreover, CSG1 and CSG2 are required for colonization of plant roots and hence these receptors – as well as glucose - play an important role for fungus-plant interaction.

As pheromone receptors were shown in Fusarium as important for plant sensing, we were interested in a potential crosstalk between glucose- and pheromone- sensing. Although CSG1 and CSG2 are dispensible for sexual development, fruiting body formation of T. reesei is accelerated in the presence of plant roots.

We conclude that T. reesei senses extracellular glucose concentrations to discriminate between degradable plant material (liberated glucose amount correlating with enzymes secreted) and the presence of a plant (secreted glucose not correlating with enzymes secreted). Upon interaction of plant roots with T. reesei fruiting bodies, the fungus recognized also the living plant as carbon source, but did not harm growth. Hence the benefit of detecting a plant can be interpreted as one reason for accelerated sexual development by the fungus to improve its interaction with the nourishing plant.