Fertility depression among cheese‐makingPenicillium roquefortistrains suggests degeneration during domestication

Abstract

Genetic differentiation occurs when gene flow is prevented, due to reproductive barriers or asexuality. Investigating the early barriers to gene flow is important for understanding the process of speciation. Here, we therefore investigated reproductive isolation between different genetic clusters of the fungus Penicillium roqueforti, used for maturing blue cheeses, and also occurring as food spoiler or in silage. We investigated premating and postmating fertility between and within three genetic clusters (two from cheese and one from other substrates), and we observed sexual structures under scanning electron microscopy. All intercluster types of crosses showed some fertility, suggesting that no intersterility has evolved between domesticated and wild populations despite adaptation to different environments and lack of gene flow. However, much lower fertility was found in crosses within the cheese clusters than within the noncheese cluster, suggesting reduced fertility of cheese strains, which may constitute a barrier to gene flow. Such degeneration may be due to bottlenecks during domestication and/or to the exclusive clonal replication of the strains in industry. This study shows that degeneration has occurred rapidly and independently in two lineages of a domesticated species. Altogether, these results inform on the processes and tempo of degeneration and speciation.

Independent domestication events in the blue-cheese fungusPenicillium roqueforti

“…There was no particular sampling bias regarding geography either (Table S1). A previous study showed that these bottlenecks, together with clonal multiplication, decreased fertility, with different stages in sexual reproduction affected in the two populations identified here as the Roquefort and non-Roquefort lineages (Ropars et al, 2016b). The non-Roquefort cheese population, despite suffering from a more severe and more recent bottleneck, was found to be used in the production of all types of blue cheese worldwide, including Gorgonzola, Bleu d’Auvergne, Stilton, Cabrales and Fourme d’Ambert.…”

Comparative genomics applied to Mucor species with different lifestyles

“…Although the different species within the Mucoromycotina subphylum are expected to produce and accumulate large amount of carotenoids, differences might exist among species [60]. Terpenes play also an important role in flavour production which is an important trait for cheese-ripening fungi that could have been under human-directed selection in species used for cheese making [61]. This study indicated that the main genes involved in terpene biosynthesis were conserved among the analysed Mucor species without any important differences in terms of gene number with the exception of GGPP genes for which the number is lower in the endophytic species as well as in M. griseocyanus and in the M. indicus opportunistic pathogen.…”

Omics Analyses of Trichoderma reesei CBS999.97 and QM6a Indicate the Relevance of Female Fertility to Carbohydrate-Active Enzyme and Transporter Levels

“…Interestingly, the female sterile mutants then released the spores they produced more efficiently, which is considered crucial for the invasion of natural populations by female sterile mutants ( 21 ). In Penicillium roqueforti , fertility also decreases during industrial use and the necessary clonal replication there ( 20 ). A similar phenomenon may have happened for QM6a, but we have isolates from natural environment that are female sterile as well.…”

“…Considering sexual development as a tool in industry, it is required that this process work reliably and continuously. However, it was shown for other fungi that asexual cultivation, which is routinely done for inoculum generation, results in the loss of female fertility ( 20 , 21 ). Also, for T. reesei QM6a, it was considered possible that its defect might be a result of repetitive laboratory cultivation ( 12 ).…”