Pheromone independent unisexual development in Cryptococcus neoformans

Rachana Gyawali,Youbao Zhao,Jianfeng Lin,Yumeng Fan,Srijana Upadhyay,Xiaorong Lin,Xinping Xu,Michael Freitag

doi:10.1371/journal.pgen.1006772

Abstract

The fungus Cryptococcus neoformans can undergo a-α bisexual and unisexual reproduction. Completion of both sexual reproduction modes requires similar cellular differentiation processes and meiosis. Although bisexual reproduction generates equal number of a and α progeny and is far more efficient than unisexual reproduction under mating-inducing laboratory conditions, the α mating type dominates in nature. Population genetic studies suggest that unisexual reproduction by α isolates might have contributed to this sharply skewed distribution of the mating types. However, the predominance of the α mating type and the seemingly inefficient unisexual reproduction observed under laboratory conditions present a conundrum. Here, we discovered a previously unrecognized condition that promotes unisexual reproduction while suppressing bisexual reproduction. Pheromone is the principal stimulus for bisexual development in Cryptococcus. Interestingly, pheromone and other components of the pheromone pathway, including the key transcription factor Mat2, are not necessary but rather inhibitory for Cryptococcus to complete its unisexual cycle under this condition. The inactivation of the pheromone pathway promotes unisexual reproduction despite the essential role of this pathway in non-self-recognition during bisexual reproduction. Nonetheless, the requirement for the known filamentation regulator Znf2 and the expression of hyphal or basidium specific proteins remain the same for pheromone-dependent or independent sexual reproduction. Transcriptome analyses and an insertional mutagenesis screen in mat2Δ identified calcineurin being essential for this process. We further found that Znf2 and calcineurin work cooperatively in controlling unisexual development in this fungus. These findings indicate that Mat2 acts as a repressor of pheromone-independent unisexual development while serving as an activator for a-α bisexual development. The bi-functionality of Mat2 might have allowed it to act as a toggle switch for the mode of sexual development in this ubiquitous eukaryotic microbe.

Highlights

Sexual reproduction is generally considered bisexual, involving partners of the opposite sex
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication
We showed that unisexual reproduction occurring under this condition is independent of pheromone or the key components of the pheromone pathway, despite the fact that this pathway is crucial for bisexual development

Summary

Introduction

Sexual reproduction is generally considered bisexual, involving partners of the opposite sex. Unisexual development (self-fertile or inbreeding) occurs in some eukaryotes without the need for an opposite mating partner [1,2,3,4]. Each reproduction mode has its own costs and benefits. But finding a compatible mating partner can be challenging. Unisexual reproduction promotes inbreeding/selfing, but it avoids the cost associated with locating a mating partner. The latter might be challenging for species that are immobile or species where compatible partners are rare

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