Maize Diterpenoid Sensing via the Ste3 A-Pheromone Receptor Guide Oval Conidia of Colletotrichum graminicola to Host Roots.

Colletotrichum graminicola, the maize anthracnose fungus, is known for its ability to invade above-ground tissues. This fungus forms two distinct asexual spore types in its life cycle, falcate conidia in acervuli on infected leaves and oval conidia in parenchyma cells in leaf and stem lesions. Our study reveals a previously unknown role for oval conidia in the infection of roots. We investigated whether root exudate from maize could redirect the growth of germlings generated by C. graminicola. Our results showed that only germlings derived from oval conidia were able to respond to root exudates, whereas those from falcate conidia did not. High-performance liquid chromatography/mass spectrometry (HPLC-MS) analyses combined with biological assays and genetic studies identified diterpenoids from maize as attractants perceived by the a-pheromone receptor CgSte3. We further explored the root-fungus interaction by analysing the germination of oval and falcate spores in soils of different composition. Oval conidia germinated rapidly under all conditions, whereas falcate conidia remained dormant and became highly vacuolated even in the presence of the host plant. Microscopic evaluation of root infection experiments showed that both conidia types attached to root material and formed penetration structures. However, only oval conidia enabled the pathogenic fungus to reach upper plant parts from infected roots. Our findings suggest a novel role for oval conidia in the infection of roots, highlighting the complexity of the anthracnose disease cycle.