Sexual reproduction likely evolved as protection from environmental stresses, specifically, to repair DNA damage, often via homologous recombination. In higher eukaryotes, meiosis and the production of gametes with allelic combinations different from parental type provides the side effect of increased genetic variation. In fungi it appears that while the maintenance of meiosis is paramount for success, outcrossing is not a driving force. In the subkingdom Dikarya, fungal members are characterized by existence of a dikaryon for extended stages within the life cycle. Such fungi possess functional or, in some cases, relictual, loci that govern sexual reproduction between members of their own species. All mating systems identified so far in the Dikarya employ a pheromone/receptor system for haploid organisms to recognize a compatible mating partner, although the paradigm in the Ascomycota, e.g., Saccharomyces cerevisiae, is that genes for the pheromone precursor and receptor are not found in the matingtype locus but rather are regulated by its products. Similarly, the mating systems in the Ascomycota are bipolar, with two non-allelic idiomorphs expressed in cells of opposite mating type. In contrast, for the Basidiomycota, both bipolar and tetrapolar mating systems have been well characterized; further, at least one locus directly encodes the pheromone precursor and the receptor for the pheromone of a different mating type, while a separate locus encodes proteins that may regulate the first locus and/or additional genes required for downstream events. Heterozygosity at both of two unlinked loci is required for cells to productively mate in tetrapolar systems, whereas in bipolar systems the two loci are tightly linked. Finally, a trade-off exists in wild fungal populations between sexual reproduction and the associated costs, with adverse conditions leading to mating. For fungal mammal pathogens, the products of sexual reproduction can be targets for the host immune system. The opposite appears true for phytopathogenic fungi, where mating and pathogenicity are inextricably linked. Here, we explore, compare, and contrast different strategies used among the Dikarya, both saprophytic and pathogenic fungi, and highlight differences between pathogens of mammals and pathogens of plants, providing context for selective pressures acting on this interesting group of fungi.
Recombination is beneficial over the long term, allowing more effective selection. Despite long-term advantages of recombination, local recombination suppression is known to evolve and lead to genomic degeneration, in particular on sex and mating-type chromosomes, sometimes linked to severe genetic diseases. Here, we investigated the tempo of degeneration in non-recombining regions, i.e., the function curve for the accumulation of deleterious mutations over time, taking advantage of 17 independent events of large recombination suppression identified on mating-type chromosomes of anther-smut fungi, including five newly identified in the present study. Using high-quality genomes assemblies of alternative mating types of 13 Microbotryum species, we estimated the degeneration levels in terms of accumulation of non-optimal codons and non-synonymous substitutions in non-recombining regions. We found a reduced frequency of optimal codons in the non-recombining regions on mating-type chromosomes compared to autosomes. We showed that the lower frequency of optimal codons in non-recombining regions was not due to less frequent GC-biased gene conversion or lower ancestral expression levels compared to recombining regions. We estimated that the frequency of optimal codon usage decreased linearly at a rate of 0.989 per My. The non-synonymous over synonymous substitution rate (dN/dS) increased rapidly after recombination suppression and then reached a plateau. To our knowledge this is the first study to disentangle effects of reduced selection efficacy from GC-biased gene conversion in the evolution of optimal codon usage to quantify the tempo of degeneration in non-recombining regions, leveraging on multiple independent recombination suppression events. Understanding the tempo of degeneration is important for our knowledge on genomic evolution, on the origin of genetic diseases and on the maintenance of regions without recombination.
Recombination is beneficial over the long term, allowing more effective selection. Despite long-term advantages of recombination, local recombination suppression can evolve and lead to genomic degeneration, in particular on sex chromosomes. Here, we investigated the tempo of degeneration in non-recombining regions, i.e., the function curve for the accumulation of deleterious mutations over time, leveraging on 22 independent events of recombination suppression identified on mating-type chromosomes of anther-smut fungi, including newly identified ones. Using previously available and newly generated high-quality genome assemblies of alternative mating types of 13 Microbotryum species, we estimated degeneration levels in terms of accumulation of non-optimal codons and non-synonymous substitutions in non-recombining regions. We found a reduced frequency of optimal codons in the non-recombining regions compared to autosomes, that was not due to less frequent GC-biased gene conversion or lower ancestral expression levels compared to recombining regions. The frequency of optimal codons rapidly decreased following recombination suppression and reached an asymptote after ca 3 Mya. The strength of purifying selection remained virtually constant at dN/dS = 0.55, i.e. at an intermediate level between purifying selection and neutral evolution. Accordingly, non-synonymous differences between mating-type chromosomes increased linearly with stratum age, at a rate of 0.015 per MY. We thus develop a method for disentangling effects of reduced selection efficacy from GC-biased gene conversion in the evolution of codon usage and we quantify the tempo of degeneration in non-recombining regions, which is important for our knowledge on genomic evolution and on the maintenance of regions without recombination.
Components of the cAMP (cyclic AMP) signalling cascades are conserved from fungi to humans, and are particularly important for fungal dimorphism and pathogenicity. Previous work has described two phosphodiesterases, UmPde1 and UmPde2, in Ustilago maydis which show strong phosphodiesterase activity. We further characterized the biological function(s) of these phosphodiesterases in U. maydis. Specifically, we examined their possible role(s) in regulation of the cAMP-dependent protein kinase A (PKA) pathway and their roles in filamentous growth and pathogenicity. We found that UmPde1, which shares 35 % similarity with Cryptococcus neoformans Pde1, also displays functional homology with this enzyme. UmPde1 complements the capsule-formation defect of C. neoformans strains deleted for Pde1. In U. maydis, the cell morphology of the umpde1 deletion mutant resembled the multiple budding phenotypes seen with the ubc1 mutant, which lacks the regulatory subunit of PKA. Interestingly, on low-ammonium medium, umpde2 deletion strains showed a reduction in filamentation that was comparable to that of ubc1 deletion strains; however, umpde1 deletion strains showed normal filamentation on lowammonium medium. Furthermore, both the ubc1 deletion strain in which the PKA pathway was constitutively active and the umpde1 deletion strains were significantly reduced in pathogenicity, while the umpde2 deletion strains showed a trend for reduced pathogenicity compared with wildtype strains. These data support a role for the phosphodiesterases UmPde1 and UmPde2 in regulating the U. maydis cAMP-dependent PKA pathway through modulation of cAMP levels, thus affecting dimorphic growth and pathogenicity.
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