Sex in Cheese: Evidence for Sexuality in the Fungus Penicillium roqueforti

Jeanne Ropars,Fabienne Malagnac,Ricardo C Rodríguez De La Vega,Eric Fontanillas,Manuela López-Villavicencio,Monika Coton,Tatiana Giraud,Joëlle Dupont,Nicolas Corradi

doi:10.1371/journal.pone.0049665

Abstract

Although most eukaryotes reproduce sexually at some moment of their life cycle, as much as a fifth of fungal species were thought to reproduce exclusively asexually. Nevertheless, recent studies have revealed the occurrence of sex in some of these supposedly asexual species. For industrially relevant fungi, for which inoculums are produced by clonal-subcultures since decades, the potentiality for sex is of great interest for strain improvement strategies. Here, we investigated the sexual capability of the fungus Penicillium roqueforti, used as starter for blue cheese production. We present indirect evidence suggesting that recombination could be occurring in this species. The screening of a large sample of strains isolated from diverse substrates throughout the world revealed the existence of individuals of both mating types, even in the very same cheese. The MAT genes, involved in fungal sexual compatibility, appeared to evolve under purifying selection, suggesting that they are still functional. The examination of the recently sequenced genome of the FM 164 cheese strain enabled the identification of the most important genes known to be involved in meiosis, which were found to be highly conserved. Linkage disequilibria were not significant among three of the six marker pairs and 11 out of the 16 possible allelic combinations were found in the dataset. Finally, the detection of signatures of repeat induced point mutations (RIP) in repeated sequences and transposable elements reinforces the conclusion that P. roqueforti underwent more or less recent sex events. In this species of high industrial importance, the induction of a sexual cycle would open the possibility of generating new genotypes that would be extremely useful to diversify cheese products.

Highlights

The maintenance of sex remains one of the most fundamental questions in evolutionary biology
Three pairs of markers were not in significant linkage disequilibria and 11 out of the 16 possible allelic combinations were found in the dataset
We did find evidence of the occurrence of recombination as 11 out of the 16 possible allelic combinations were found in our dataset, and three of the six marker pairs did not display significant linkage disequilibria

Summary

Introduction

The maintenance of sex remains one of the most fundamental questions in evolutionary biology. When males contribute little or no resources to their progeny, a mutation causing females to reproduce asexually is expected to thrive because its frequency doubles at each generation (which is known as the ‘twofold cost of sex’) [1]. Various additional costs associated with mating apply to more specific cases, including costs of finding and courting a mate, risks of predation, of contracting sexually transmitted diseases or parasitic genetic elements [2]. Despite these heavy costs, most eukaryotes engage in sexual recombination at least at some point in their life cycle. It can lead to a more rapid adaptive response by bringing together beneficial mutations, allowing their fixation in the populations, especially in harsh environments where selection is strong [5,9,10]

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Discussion

Conclusion