It's All in the Genes: The Regulatory Pathways of Sexual Reproduction in Filamentous Ascomycetes

Abstract

Sexual reproduction in filamentous ascomycete fungi results in the production of highly specialized sexual tissues, which arise from relatively simple, vegetative mycelia. This conversion takes place after the recognition of and response to a variety of exogenous and endogenous cues, and relies on very strictly regulated gene, protein, and metabolite pathways. This makes studying sexual development in fungi an interesting tool in which to study gene-gene, gene-protein, and protein-metabolite interactions. This review provides an overview of some of the most important genes involved in this process; from those involved in the conversion of mycelia into sexually-competent tissue, to those involved in the development of the ascomata, the asci, and ultimately, the ascospores.

Keywords: filamentous ascomycetes; functional characterisation; fungi; gene expression; regulatory networks; sexual reproduction.

Figure 1

Generalized sexual cycle of filamentous ascomycetes. Mycelial strands (1) recognize a variety of signals before being converted into sexually competent tissue. One such signal is the recognition of a suitable mating partner. One partner produces the female structure, an ascogonium (indicated by the structure with red nuclei), while the second partner produces fertilizing spermatia (indicated by the single cells with blue nuclei). Gamete fertilization (2) occurs when the spermatia physically interact with the ascogonium. This is followed by the production of the protoascomata (3). Stages (4) to (8) occur within the immature ascomata and the developing asci. This includes the development of a crozier, nuclear migration, karyogamy, meiosis, and mitosis. This entire process culminates in a fully mature ascoma (9), which can release ascospores (10). These spores will then germinate and begin the cycle again.

Figure 2

The sexual strategies of filamentous ascomycetes. Heterothallism: Two isolates of an opposite mating type need to physically interact in order to produce sexual structures. These mating types are genetically determined by genes at the MAT locus, either encoding the MAT1-1 genes (red) or the MAT1-2 genes (blue). These genes confer the MAT1-1 and MAT1-2 mating identities, respectively. Homothallism: Sexual reproduction can either occur within a single isolate that expresses both the MAT1-1 and MAT1-2 genes (as illustrated) or between any two individuals of the same species.

Figure 3

The involvement of the cross-pathway regulatory network (CPRN) during sexual reproduction in A. nidulans. In the absence of amino acids, cpcA is up-regulated, thereby activating the CPRN. This pathway subsequently inhibits the onset of sexual reproduction. In contrast, when amino acids are available, cpcB is up-regulated and the CPRN is inhibited. This results in sexual development. Either the overexpression of cpcA or the deletion of cpcB can activate the CPRN, by simulating amino acid deficiency, and thus also inhibit sexual reproduction. Shapes with green outlines indicate conditions under which sexual reproduction is directly or indirectly activated. Those with red outlines indicate conditions which directly or indirectly repress sexual reproduction. Green arrows indicate activation of a particular pathway, while red lines terminating in circles indicate repression.

Figure 4

Sexual reproduction and light sensing in A. nidulans. Darkness: VeA and VelB interact with the importin protein, KapA. This allows their transport into the nucleus where they regulate gene expression and initiate sexual development. Light: FphA, the red light sensor, interacts with VeA, putatively inhibiting its interaction with KapA and VelB. This prevents the transport of VeA into the nucleus. Instead, VelB interacts with other proteins, activating asexual reproduction.

Figure 5

Pheromone signalling in heterothallic filamentous ascomycetes. (1) Pheromones are expressed, with spermatia of MAT1-1 isolates expressing the α-factor and spermatia of MAT1-2 isolates expressing the a-factor pheromone. (2) The ascogonia of these isolates also express the pheromone receptors, which recognize the pheromones. (3) Recognition of the pheromones by their receptors results in a variety of physiological changes, including growth towards the suitable partner as well as the transcriptional regulation of sex-related genes.