Basidiomycete mating type genes and pheromone signaling

Abstract

The genome sequences of the basidiomycete Agaricomycetes species Coprinopsis cinerea, Laccaria bicolor, Schizophyllum commune, Phanerochaete chrysosporium, and Postia placenta, as well as of Cryptococcus neoformans and Ustilago maydis, are now publicly available. Out of these fungi, C. cinerea, S. commune, and U. maydis, together with the budding yeast Saccharomyces cerevisiae, have been investigated for years genetically and molecularly for signaling in sexual reproduction. The comparison of the structure and organization of mating type genes in fungal genomes reveals an amazing conservation of genes regulating the sexual reproduction throughout the fungal kingdom. In agaricomycetes, two mating type loci, A, coding for homeodomain type transcription factors, and B, encoding a pheromone/receptor system, regulate the four typical mating interactions of tetrapolar species. Evidence for both A and B mating type genes can also be identified in basidiomycetes with bipolar systems, where only two mating interactions are seen. In some of these fungi, the B locus has lost its self/nonself discrimination ability and thus its specificity while retaining the other regulatory functions in development. In silico analyses now also permit the identification of putative components of the pheromone-dependent signaling pathways. Induction of these signaling cascades leads to development of dikaryotic mycelia, fruiting body formation, and meiotic spore production. In pheromone-dependent signaling, the role of heterotrimeric G proteins, components of a mitogen-activated protein kinase (MAPK) cascade, and cyclic AMP-dependent pathways can now be defined. Additionally, the pheromone-dependent signaling through monomeric, small GTPases potentially involved in creating the polarized cytoskeleton for reciprocal nuclear exchange and migration during mating is predicted.

Fig. 1.

Life cycle of the tetrapolar basidiomycete Schizophyllum commune. In the fruiting bodies, basidiospores with four different combinations of A and B mating type genes are produced. If both A and B genes are different in two developing, haploid mycelia, a fully compatible mating takes place. (1) B genes regulate the reciprocal nuclear migration, illustrated by movement of a nucleus via a hyphal fusion through broken septa from one haploid hypha into the other. (2) As a consequence of nuclear migration, multinucleate hyphae occur in the interaction zone of the mates. Unfused clamp connections (pseudoclamps) in the multinucleate hyphae are seen as a function of A-regulated development (3), which then controls the pairing of different nuclei followed by the hook cell formation and synchronous nuclear division (4). After separation of the sister nuclei, a cross wall is formed at the base of the hook and in the hypha (5). The growth of the hook toward and the subsequent fusion to the subapical cell are controlled by B genes and allow the movement of the nucleus from the hook into the subapical cell to complete clamp formation (6).

Fig. 2.

Putative signaling components in fungal mating interactions. (A) The well-known components of the signaling pathway associated with mating in the ascomycete S. cerevisiae (78) and in the ustilaginomycete U. maydis (126), as well as the known and putative signaling in the agaricomycete S. commune, are shown. The arrows illustrate the direction of signaling from pheromone/receptor interaction via G protein and MAPK cascade to the transcription factor (TF). Note that in S. cerevisiae the Ste4/18 (βγ) complex interacts with Ste20 (a PAK-like kinase), which then signals further to the MAPK cascade containing the scaffolding protein Ste5. No Ste5 has been found in the S. commune genome, while an ortholog to Ste20 is detected. A homolog to Ste50, involved in mating response, invasive/filamentous growth, and osmotolerance, and acting as an adaptor that links the G protein-associated Cdc42-Ste20 complex to Ste11 in S. cerevisiae, has been identified in U. maydis (Ubc2 [46]) and in S. commune. (B) A hypothetical model of signaling components in the agaricomycete S. commune after G protein activation by pheromone/receptor interaction. The released G protein subunits activate a homologous MAPK cascade. Perceived functions include induction of enzymes necessary for hyphal fusions and septal dissolution, which might also respond to the cAMP-dependent Pka pathway. In addition to the MAPK cascade, Gβγ has been shown to activate Cdc42, thus controlling cytoskeletal rearrangement necessary for nuclear exchange and migration.