Genetic Networks That Govern Sexual Reproduction in the Pezizomycotina

Abstract

Sexual development in filamentous fungi is a complex process that relies on the precise control of and interaction between a variety of genetic networks and pathways. The mating-type (MAT) genes are the master regulators of this process and typically act as transcription factors, which control the expression of genes involved at all stages of the sexual cycle. In many fungi, the sexual cycle typically begins when the mating pheromones of one mating type are recognized by a compatible partner, followed by physical interaction and fertilization. Subsequently, highly specialized sexual structures are formed, within which the sexual spores develop after rounds of meiosis and mitosis. These spores are then released and germinate, forming new individuals that initiate new cycles of growth. This review provides an overview of the known genetic networks and pathways that are involved in each major stage of the sexual cycle in filamentous ascomycete fungi.

Keywords: MAT genes; Pezizomycotina; fertility; pheromones; sexual reproduction.

FIG 1

Generalized sexual cycle of heterothallic Pezizomycotina fungi. The cycle begins (step 1) with an interaction between compatible isolates, with male structures from one of the partners secreting pheromones (step 2), which are recognized by the female structures from a suitable mating partner (step 3). This recognition results in growth of the trichogyne toward the male cells (step 4), resulting in physical contact between the two partners; fertilization (step 5); and the subsequent production of a protoascoma (step 6). Within the ascus, multiple rounds of meiosis and mitosis produce the mature ascospores (steps 7 to 12), which are subsequently released (step 13) from the mature ascoma (step 14). This cycle would be identical in homothallic species, except that an opposite mating partner would not be required to initiate the process. The different ascomatal types are depicted below the sexual cycle, illustrating the morphological diversity that can be observed in the Pezizomyctonia.

FIG 2

Mating-type idiomorphs, MAT genes, and their distribution in fungi utilizing the various sexual strategies exhibited by Pezizomycotina fungi. Open circles represent nuclei in each cell, while closed circles represent the ascospores produced. Red indicates the presence of genes from the MAT1-1 idiomorph, and blue indicates the presence of genes from the MAT1-2 idiomorph.

FIG 3

Cladogram of the Pezizomycotina highlighting the lack of studies on sexual reproduction in this group. Classes or orders shown in red have no described MAT genes and/or no published functional studies relating to the sexual process. Orders shown in white have at least one species with described MAT genes and/or at least one functional study related to sexual reproduction. Details can be found in Table S1 in the supplemental material. The cladogram was constructed in phyloT using NCBI taxonomic identification numbers and was edited in iTol v6 (https://itol.embl.de/).

FIG 4

Pheromone response pathway in Neurospora crassa. The MAT1-1-1 and MAT1-2-1 proteins control the expression of the α- and a-factor pheromones, respectively. Recognition of the pheromones by their respective cognate receptors results in activation of the coupled G-protein and dissociation of its subunits. These subunits subsequently activate one of the three MAPK cascades, MAK2, that ultimately results in protoascomatal development. Two other MAPK cascades, MAK1 and OS-2, are also important for protoascomatal development but respond to different environmental signals.

FIG 5

Structure and processing of a- and α-factor mating pheromones. Both fungal mating pheromones are initially expressed as large preproteins which are processed into small, mature pheromone factors. The first step in the processing of the a-factor includes the addition of a farnesyl (indicated by the “+” symbol) by RAM1/RAM2. This is followed by cleavage of the terminal AAX amino acids by RCE1/STE24 and the addition of a carboxymethyl group (indicated by a hexagon symbol) by STE14. Two final cleavage events, facilitated by STE24 and AXL1, release the mature pheromone. The first step in α-factor processing is the removal of the signal peptide (indicated in dark orange). KEX2-, KEX1-, and STE13-mediated cleavage releases numerous copies of the mature pheromone.

FIG 6

Important protein complexes and pathways involved in protoascomatal maturation and ascomatal development in various filamentous fungi. (A) The STRIPAK is important for sexual development in the homothallic Sordaria macrospora. (Based on data from reference .) (B) The PACC pathway plays an essential role in protoascomatal development in the heterothallic Neurospora crassa. (Adapted from reference .) (C) The COP9 signalosome is important for sexual development and other developmental processes in the homothallic Aspergillus nidulans. (Based on data from references and .) Protein names and/or abbreviations: GPI1 (glycosylphosphatidylinositol-anchored protein); MOB3 (monopolar spindle one-binder protein); PP2Ac and PP2Aa (protein phosphatase subunits); KIN3 and KIN24 (kinases 3 and 24); CLA4 (from the p21-activated kinase family); PALA, PALB, PALC, PALF, and PALH (various proteins from the PAL/RIM pathway); PACC (terminal transcription factor of the PACC pathway); and CSN1-8 (COP9 signalosome proteins 1 to 8).