Abstract

In fungi belonging to the phylum Basidiomycota, sexual compatibility is usually determined by two genetically unlinked MAT loci, one of which encodes one or more pheromone receptors (P/R) and pheromone precursors, and the other comprehends at least one pair of divergently transcribed genes encoding homeodomain (HD) transcription factors. Most species are heterothallic, meaning that sexual reproduction requires mating between two sexually compatible individuals harboring different alleles at both MAT loci. However, some species are known to be homothallic, one individual being capable of completing the sexual cycle without mating with a genetically distinct partner. While the molecular underpinnings of the heterothallic life cycles of several basidiomycete model species have been dissected in great detail, much less is known concerning the molecular basis for homothallism. Following the discovery in available draft genomes of the homothallic basidiomycetous yeast Phaffia rhodozyma of P/R and HD genes, we employed available genetic tools to determine their role in sexual development. Two P/R clusters, each harboring one pheromone receptor and one pheromone precursor gene were found in close vicinity of each other and were shown to form two redundant P/R pairs, each receptor being activated by the pheromone encoded by the most distal pheromone precursor gene. The HD locus is apparently genetically unlinked to the P/R locus and encodes a single pair of divergently transcribed HD1 and HD2 transcription factors, both required for normal completion of the sexual cycle. Given the genetic makeup of P. rhodozyma MAT loci, we postulate that it is a primarily homothallic organism and we propose a model for the interplay of molecular interactions required for sexual development in this species. Phaffia rhodozyma is considered one of the most promising microbial source of the carotenoid astaxanthin. Further development of this yeast as an industrial organism will benefit from new insights regarding its sexual reproduction system.

Highlights

  • The ability to reproduce sexually is a widespread trait in all eukaryotic lineages and it is pervasive in fungi, where key regulators of sexual behavior are encoded in specialized chromosomal regions named MAT loci [1]

  • Some fungi are capable of sexual reproduction without the need for a sexually compatible partner, a behavior called homothallism

  • A feature common so far to all fungal mating systems seems to be the involvement of mating type specific transcription factors that contribute to post-mating sexual development [1]

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Summary

Introduction

The ability to reproduce sexually is a widespread trait in all eukaryotic lineages and it is pervasive in fungi, where key regulators of sexual behavior are encoded in specialized chromosomal regions named MAT loci [1]. Mating in fungi is governed by mechanisms of self/non-self recognition, and it usually involves two individuals that carry different alleles at the respective MAT loci and belong to distinct mating types. In Ascomycota and in the early derived Zygomycota, MAT identity is defined at a single locus that encodes one of two possible, very dissimilar idiomorphic sequences. In these two lineages, mating systems have so far been found to be bipolar, which means that that they have a single MAT locus and spores belonging to two distinct mating types may arise after meiosis [1,2]. Each type of haploid cell expresses only one type of pheromone and one type of pheromone receptor, which define their sexual identity and promote mate recognition and cell fusion [5,6,7]

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