Sexual reproduction and mating-type–mediated strain development in the penicillin-producing fungus Penicillium chrysogenum

Abstract

Penicillium chrysogenum is a filamentous fungus of major medical and historical importance, being the original and present-day industrial source of the antibiotic penicillin. The species has been considered asexual for more than 100 y, and despite concerted efforts, it has not been possible to induce sexual reproduction, which has prevented sexual crosses being used for strain improvement. However, using knowledge of mating-type (MAT) gene organization, we now describe conditions under which a sexual cycle can be induced leading to production of meiotic ascospores. Evidence of recombination was obtained using both molecular and phenotypic markers. The identified heterothallic sexual cycle was used for strain development purposes, generating offspring with novel combinations of traits relevant to penicillin production. Furthermore, the MAT1-1-1 mating-type gene, known primarily for a role in governing sexual identity, was also found to control transcription of a wide range of genes with biotechnological relevance including those regulating penicillin production, hyphal morphology, and conidial formation. These discoveries of a sexual cycle and MAT gene function are likely to be of broad relevance for manipulation of other asexual fungi of economic importance.sexual recombination | secondary metabolism | ascomycete

Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential

“…In addition to the remodelling of the fungal wall, the endobacterium affects the expression of genes containing the mating type domains (Supplementary Table S1 and S2), raising the question whether these genes could be involved in the production of the asexual conidia, as reported for Penicillium chrysogenum (Bohm et al, 2013). To test whether the presence of the bacteria affected spore formation, we monitored the spore production of G. margarita over 3 years (Supplementary Table S6) and found that the cured line produced only the 50% of the spores produced by the G. margarita line containing the bacteria.…”

The Transition from a Phytopathogenic Smut Ancestor to an Anamorphic Biocontrol Agent Deciphered by Comparative Whole-Genome Analysis

“…The presence in the P. flocculosa genome of all other genes shown to be necessary for the initiation of mating, maintenance of the dikaryotic pathogenic state, and meiosis in U. maydis suggests that P. flocculosa is either capable of mating and sex under certain circumstances or has recently lost this capability. One would expect that selection pressure would alter the presence or function of mating genes in strict anamorphs, but recent genome sequence analyses have shown that fungal species reproducing asexually in nature possessed all genes involved in sexual reproduction and were even capable of mating under in vitro conditions (Xu et al, 2007;O'Gorman et al, 2009;Böhm et al, 2013). Interestingly, P. flocculosa does not require mating to unleash its pathogenic potential onto mildew fungi, although this mechanism of epiphytic competition is likely different from the host infection requirement of the smuts.…”

Global Gene Expression and Focused Knockout Analysis Reveals Genes Associated with Fungal Fruiting Body Development in Neurospora crassa

“…In Neurospora and other fungal species, mating type idiomorphs impact diverse genes that are not directly involved in the mating process (21,23,45,59,60). The increased expression of mat a-1 and ccg-4 that we observed during sexual development of N. crassa calls for further investigation using strain-specific expression assays conducted with varied crosses.…”

“…However, the sexual growth of N. crassa arises as a consequence of a communion of cells of different nuclear types; the heterokaryotic reproductive cells develop into sterile paraphyses within the perithecium or undergo karyogamy and a short diploid phase prior to the production of haploid ascospores. This heterokaryosis has made it challenging to study sexual differentiation using traditional methods based on genetic screens for mutants (13,14), and genome-wide assays so far have yielded only limited information about the genetics underlying the production of multicellular sexual reproduction structures such as perithecia (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23).…”

“…In animals and plants, analyses of gene expression and genetic regulatory networks in model organisms have demonstrated that genes work together in response to regulatory factors to shape metabolic processes and morphological development (2,4,23,26,27). N. crassa has evolved various mechanisms to ensure proper development during premating, mating, and postmating stages based on heterokaryotic and protoplasmic incompatibility, signaling, silencing, and secondary metabolism pathways.…”