Maintaining Two Mating Types: Structure of the Mating Type Locus and Its Role in Heterokaryosis inPodospora anserina

Abstract

Pseudo-homothallism is a reproductive strategy elected by some fungi producing heterokaryotic sexual spores containing genetically different but sexually compatible nuclei. This lifestyle appears as a compromise between true homothallism (self-fertility with predominant inbreeding) and complete heterothallism (with exclusive outcrossing). However, pseudohomothallic species face the problem of maintaining heterokaryotic mycelia to fully benefit from this lifestyle, as homokaryons are self-sterile. Here, we report on the structure of chromosome 1 in mat+ and mat2 isolates of strain S of the pseudohomothallic fungus Podospora anserina. Chromosome 1 contains either one of the mat+ and mat2 mating types of P. anserina, which is mostly found in nature as a mat+/mat2 heterokaryotic mycelium harboring sexually compatible nuclei. We identified a "mat" region 0.8 Mb long, devoid of meiotic recombination and containing the mating-type idiomorphs, which is a candidate to be involved in the maintenance of the heterokaryotic state, since the S mat+ and S mat2 strains have different physiology that may enable hybrid-vigor-like phenomena in the heterokaryons. The mat region contains 229 coding sequences. A total of 687 polymorphisms were detected between the S mat+ and S mat2 chromosomes. Importantly, the mat region is colinear between both chromosomes, which calls for an original mechanism of recombination inhibition. Microarray analyses revealed that 10% of the P. anserina genes have different transcriptional profiles in S mat+ and S mat2, in line with their different phenotypes. Finally, we show that the heterokaryotic state is faithfully maintained during mycelium growth of P. anserina, yet mat+/mat+ and mat2/mat2 heterokaryons are as stable as mat+/mat2 ones, evidencing a maintenance of heterokaryosis that does not rely on fitness-enhancing complementation between the S mat+ and S mat2 strains.A dikaryotic stage during a significant portion of the lifecycle is the hallmark of the higher fungi (Ascomycota and Basidiomycota), called for this reason the Dikarya. The dikaryotic part of the life cycle is different in the two groups. In Basidiomycota, mating-competent mycelia fuse and yield the secondary dikaryotic mycelium, upon which basidiosporebearing dikaryotic fruiting bodies are differentiated. In Ascomycota, fruiting bodies are differentiated around a monokaryotic female gametangium (the ascogonium), which is fertilized by a male gamete (antheridium or spermatium) to yield the dikaryon, which undergoes further development and produces numerous ascospore-containing asci. In Ascomycota, the dikaryotic stage is thus restricted to the sexual lineage inside the fruiting body. There is one exception to this in the Taphrinomycetes, where a dikaryotic mycelium is formed as part of the life cycle (Martin 1940). Ascomycota are nonetheless able to exhibit heterokaryotic mycelia following somatic fusion between genetically different individuals (Buller 1933). In Basidiomycota, a special structure (the clamp) enables the mai...

Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism

“…S2). Mating-type loci linkage has been reported in several fungi (9,14,41,42), and our study provides clues to the chromosomal rearrangements underlying this phenomenon. The five other M. lychnidis-dioicae evolutionary strata (purple, blue, orange, red, and green strata) did not involve mating-type genes.…”

Inactivation of Cellobiose Dehydrogenases Modifies the Cellulose Degradation Mechanism of Podospora anserina

“…As in previous analyses of the first version of the P. anserina genome sequence (12), analysis of a corrected version of the complete genome of P. anserina (32) revealed the presence of three sequences potentially coding for CDHs, Pa_7_2650 or P. anserina CDH1 (PaCDH1) (formerly CDHpa) (12), Pa_0_280 or PaCDH2 (formerly PaCDHB) (13), and Pa_6_11360 or PaCDH3 (Fig. 1).…”

“…The strains used in this study derived from the S wild-type strain (48) used for sequencing (30,32). Standard culture conditions, media, and genetic methods for P. anserina have been described (29,49).…”

Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma

“…Recombination suppression on the chromosome carrying the mating-type locus has evolved independently in several fungal species distantly related to N. tetrasperma, including Podospora, Cryptococcus, and Microbotryum (Fraser and Heitman 2004;Grognet et al 2014;Fontanillas et al 2015) and contributes to our understanding of different aspects of eukaryote genome evolution. Signatures of molecular degeneration associated with recombination suppression have been reported in Neurospora and Microbotryum (Hood et al 2004;Fontanillas et al 2015).…”