Abstract
BackgroundMating-type loci in yeasts and ascomycotan filamentous fungi (Pezizomycotina) encode master transcriptional factors that play a critical role in sexual development. Genome-wide analyses of mating-type-specification circuits and mating-type target genes are available in Saccharomyces cerevisiae and Schizosaccharomyces pombe; however, no such analyses have been performed in heterothallic (self-incompatible) Pezizomycotina. The heterothallic fungus Podospora anserina serves as a model for understanding the basic features of mating-type control. Its mat+ and mat− mating types are determined by dissimilar allelic sequences. The mat− sequence contains three genes, designated FMR1, SMR1 and SMR2, while the mat+ sequence contains one gene, FPR1. FMR1 and FPR1 are the major regulators of fertilization, and this study presents a genome-wide view of their target genes and analyzes their target gene regulation.Methodology/Principal FindingsThe transcriptomic profiles of the mat+ and mat− strains revealed 157 differentially transcribed genes, and transcriptomic analysis of fmr1− and fpr1− mutant strains was used to determine the regulatory actions exerted by FMR1 and FPR1 on these differentially transcribed genes. All possible combinations of transcription repression and/or activation by FMR1 and/or FPR1 were observed. Furthermore, 10 additional mating-type target genes were identified that were up- or down-regulated to the same level in mat+ and mat− strains. Of the 167 genes identified, 32 genes were selected for deletion, which resulted in the identification of two genes essential for the sexual cycle. Interspecies comparisons of mating-type target genes revealed significant numbers of orthologous pairs, although transcriptional profiles were not conserved between species.Conclusions/SignificanceThis study represents the first comprehensive genome-wide analysis of mating-type direct and indirect target genes in a heterothallic filamentous fungus. Mating-type transcription factors have many more target genes than are found in yeasts and exert a much greater diversity of regulatory actions on target genes, most of which are not directly related to mating.
Highlights
Sexual reproduction is driven by specific gene expression programs required for identifying a sexually compatible partner, mating, meiosis and generation of progeny
The quantification cycle (Cq) values for FMR1 and FPR1 cDNAs were very high at 24 h, indicating that their expression was very low at the beginning of vegetative growth (Table S1)
Subsequent genetic studies indicated that the repressor activity of each transcription factor may operate at the level of post-transcriptional pheromone maturation ([13] and reviewed in [3]). In agreement with this prediction, our study indicated that the protein-S-isoprenylcysteine O-methyltransferase (Pa_7_9690), which is required for the maturation of the lipophilic pheromone in yeast [48], is activated by FPR1 and repressed by FMR1
Summary
Sexual reproduction is driven by specific gene expression programs required for identifying a sexually compatible partner, mating, meiosis and generation of progeny. Regulation of the genes involved in the identification of the mating partner and mating is well understood at a genome-wide level in the budding yeast Saccharomyces cerevisiae [1] and the fission yeast Schizosaccharomyces pombe [2], and these analyses have identified a limited number of cell specific-genes, most of which have a known function. In contrast to the yeasts, Pezizomycotina develop complex female organs and most heterothallic (selfincompatible) fungi produce male cells, which can fertilize the female organs of the opposite mating type. This fertilization event relies on pheromone receptor systems, which resemble the archetypal system of peptidic pheromones found in the budding yeast [13,14,15,16,17,18]. FMR1 and FPR1 are the major regulators of fertilization, and this study presents a genome-wide view of their target genes and analyzes their target gene regulation
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