Fungal dialogs: intra- and interspecies communication in filamentous fungi

In many filamentous fungi, germinating spores undergo mutual attraction and fusion, thereby forming a supracellular network, which further develops into the mycelial colony. Within mature colonies, hyphal branches merge thereby increasing interconnectedness. Germling and hyphal fusion in Neurospora crassa employ an unusual signaling mechanism, in which the two fusion partners take turns in signal sending and receiving. The highly coordinated cellular behavior is mediated by an intricate signaling network, which includes two MAP kinase cascades and fungal specific factors, such as the SO protein. Function and activity of these proteins are highly dependent on their subcellular localization, indicated by the alternating membrane recruitment of the MAK-2 MAP kinase and SO during the tropic cellular interaction.

Recent studies identified SIP-1, a protein of unknown function, as an interaction partner of SO. While both proteins co-localize during the cell-cell interaction, their dynamics differ in isolated non-interacting germlings. While SO is fully cytoplasmic under these conditions, SIP-1 localizes to the plasma membrane of the growing germ tube in an alternating manner comparable to the dynamics during cell fusion. These observations indicate that germlings rapidly alternate between two physiological stages, which are probably associated with the initiation of cell-cell interactions.

In addition, we recently found that the cell-cell communication mechanism first described in N. crassa is highly conserved in the phytopathogenic grey mold Botrytis cinerea. During germling fusion, the MAK-2 and SO homologs of this fungus show dynamics identical to the ones observed in the red bread mold. Germinating spores of N. crassa and B. cinerea readily undergo interspecies interactions, suggesting that also the so far unknown signals and receptors are conserved. Interestingly, germling fusion in B. cinerea is fully absent during growth on plant surfaces, which induce pathogenic development, suggesting that cell fusion and host infection are two alternative, mutually exclusive developmental routes.