Onset and stepwise extensions of recombination suppression are common in mating-type chromosomes of Microbotryum anther-smut fungi

Sex chromosomes and mating-type chromosomes can display large genomic regions without recombination. Recombination suppression often extended stepwise with time away from the sex- or mating-type-determining genes, generating evolutionary strata of differentiation between alternative sex or mating-type chromosomes. In anther-smut fungi of the Microbotryum genus, recombination suppression evolved repeatedly, linking the two mating-type loci and extended multiple times in regions distal to the mating-type genes. Here, we obtained high-quality genome assemblies of alternative mating types for four Microbotryum fungi. We found an additional event of independent chromosomal rearrangements bringing the two mating-type loci on the same chromosome followed by recombination suppression linking them. We also found, in a new clade analysed here, that recombination suppression between the two mating-type loci occurred in several steps, with first an ancestral recombination suppression between one of the mating-type locus and its centromere; later, completion of recombination suppression up to the second mating-type locus occurred independently in three species. The estimated dates of recombination suppression between the mating-type loci ranged from 0.15 to 3.58 million years ago. In total, this makes at least nine independent events of linkage between the mating-type loci across the Microbotryum genus. Several mating-type locus linkage events occurred through the same types of chromosomal rearrangements, where similar chromosome fissions at centromeres represent convergence in the genomic changes leading to the phenotypic convergence. These findings further highlight Microbotryum fungi as excellent models to study the evolution of recombination suppression.

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1701658114 ◽

2017 ◽

Vol 114 (27) ◽

pp. 7067-7072 ◽

Cited By ~ 47

Author(s):

Sara Branco ◽

Hélène Badouin ◽

Ricardo C. Rodríguez de la Vega ◽

Jérôme Gouzy ◽

Fantin Carpentier ◽

...

Keyword(s):

Mating Type ◽

Balancing Selection ◽

Smut Fungi ◽

Mating Types ◽

Sexual Antagonism ◽

Recombination Suppression ◽

Ancestral Gene ◽

Anther Smut ◽

Mating Type Genes ◽

Suppressed Recombination

Sex chromosomes can display successive steps of recombination suppression known as “evolutionary strata,” which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9–2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of mating-type genes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution, incorporating, for example, the influence of partially linked deleterious mutations and the maintenance of neutral rearrangement polymorphism due to balancing selection on sexes and mating types.

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Higher Gene Flow in Sex-Related Chromosomes than in Autosomes during Fungal Divergence

Molecular Biology and Evolution ◽

10.1093/molbev/msz252 ◽

2019 ◽

Vol 37 (3) ◽

pp. 668-682 ◽

Cited By ~ 6

Author(s):

Fanny E Hartmann ◽

Ricardo C Rodríguez de la Vega ◽

Pierre Gladieux ◽

Wen-Juan Ma ◽

Michael E Hood ◽

...

Keyword(s):

Gene Flow ◽

Mating Type ◽

Sex Chromosomes ◽

Smut Fungi ◽

Effective Population ◽

Closely Related Species ◽

Fungal Mating ◽

Anther Smut ◽

Genomic Regions

Abstract Nonrecombining sex chromosomes are widely found to be more differentiated than autosomes among closely related species, due to smaller effective population size and/or to a disproportionally large-X effect in reproductive isolation. Although fungal mating-type chromosomes can also display large nonrecombining regions, their levels of differentiation compared with autosomes have been little studied. Anther-smut fungi from the Microbotryum genus are castrating pathogens of Caryophyllaceae plants with largely nonrecombining mating-type chromosomes. Using whole genome sequences of 40 fungal strains, we quantified genetic differentiation among strains isolated from the geographically overlapping North American species and subspecies of Silene virginica and S. caroliniana. We inferred that gene flow likely occurred at the early stages of divergence and then completely stopped. We identified large autosomal genomic regions with chromosomal inversions, with higher genetic divergence than the rest of the genomes and highly enriched in selective sweeps, supporting a role of rearrangements in preventing gene flow in genomic regions involved in ecological divergence. Unexpectedly, the nonrecombining mating-type chromosomes showed lower divergence than autosomes due to higher gene flow, which may be promoted by adaptive introgressions of less degenerated mating-type chromosomes. The fact that both mating-type chromosomes are always heterozygous and nonrecombining may explain such patterns that oppose to those found for XY or ZW sex chromosomes. The specific features of mating-type chromosomes may also apply to the UV sex chromosomes determining sexes at the haploid stage in algae and bryophytes and may help test general hypotheses on the evolutionary specificities of sex-related chromosomes.

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MITOTIC CHROMOSOME LOSS IN A DISOMIC HAPLOID OF SACCHAROMYCES CEREVISIAE

Genetics ◽

10.1093/genetics/79.3.383 ◽

1975 ◽

Vol 79 (3) ◽

pp. 383-396

Author(s):

D A Campbell ◽

S Fogel ◽

K Lusnak

Keyword(s):

Saccharomyces Cerevisiae ◽

Mating Type ◽

Mitotic Chromosome ◽

Marker Genes ◽

Chromosome Loss ◽

Type Locus ◽

Group Iii ◽

Mating Type Locus ◽

Independent Events ◽

Spontaneous Chromosome

ABSTRACT Experiments designed to characterize the incidence of mitotic chromosome loss in a yeast disomic haploid were performed. The selective methods employed utilize the non-mating property of strains disomic for linkage group III and heterozygous at the mating type locus. The principal findings are: (1) The frequency of spontaneous chromosome loss in the disome is of the order 10-4 per cell; this value approximates the frequency in the same population of spontaneous mitotic exchange resulting in homozygosity at the mating type locus. (2) The recovered diploids are pure clones, and thus represent unique events in the disomic haploid. (3) Of the euploid chromosomes recovered after events leading to chromosome loss, approximately 90% retain the parental marker configuration expected from segregation alone; however, the remainder are recombinant for marker genes, and are the result of mitotic exchanges in the disome, especially in regions near the centromere. The recombinant proportion significantly exceeds that expected if chromosome loss and mitotic exchange in the disome were independent events. The data are consistent with a model proposing mitotic nondisjunction as the event responsible for chromosome loss in the disomic haploid.

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Consequences of recombination for the evolution of the mating type locus in Chlamydomonas reinhardtii

10.1101/565275 ◽

2019 ◽

Cited By ~ 1

Author(s):

Ahmed R. Hasan ◽

Jaspreet K. Duggal ◽

Rob W. Ness

Keyword(s):

Chlamydomonas Reinhardtii ◽

Gene Conversion ◽

Mating Type ◽

Sex Chromosomes ◽

Purifying Selection ◽

Recombination Suppression ◽

Type Locus ◽

Mating Type Locus ◽

Sexual Characteristics ◽

Population Genetic Variation

SummaryRationaleRecombination suppression in sex chromosomes and mating type loci can lead to degeneration due to reduced selection efficacy and Muller’s ratchet effects. However, genetic exchange in the form of non-crossover gene conversions may still take place within crossover-suppressed regions. Recent work has found evidence that gene conversion may explain the low levels of allelic differentiation in the dimorphic mating type locus (MT) of the isogamous alga Chlamydomonas reinhardtii. However, no one has tested whether gene conversion is sufficient to avoid the degeneration of functional sequence within MT.MethodsHere, we calculate levels of linkage disequilibrium (LD) across MT as a proxy for recombination rate and investigate its relationship to patterns of population genetic variation and the efficacy of selection in the region.ResultsWe find that levels of LD predict selection efficacy across MT, and that purifying selection is stronger in shared genes than MT-limited genes to the point of being equivalent to that of autosomal genes.ConclusionsWe argue that isogamous systems without secondary sexual characteristics exhibit reduced selective pressure to differentiate sex chromosomes, and that recombination via gene conversion plays an important role in both reducing differentiation and preventing degeneration of crossover suppressed mating type loci.

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Size variation of the non-recombining region on the mating-type chromosomes in the fungal Podospora anserina species complex

Molecular Biology and Evolution ◽

10.1093/molbev/msab040 ◽

2021 ◽

Author(s):

Fanny E Hartmann ◽

S Lorena Ament-Velásquez ◽

Aaron A Vogan ◽

Valérie Gautier ◽

Stephanie Le Prieur ◽

...

Keyword(s):

Mating Type ◽

Sex Chromosomes ◽

Chromosomal Rearrangements ◽

Size Variation ◽

Sequence Divergence ◽

Podospora Anserina ◽

Strong Linkage Disequilibrium ◽

Mating Types ◽

Type Locus ◽

Mating Type Locus

Abstract Sex chromosomes often carry large non-recombining regions that can extend progressively over time, generating evolutionary strata of sequence divergence. However, some sex chromosomes display an incomplete suppression of recombination. Large genomic regions without recombination and evolutionary strata have also been documented around fungal mating-type loci, but have been studied in only a few fungal systems. In the model fungus Podospora anserina (Ascomycota, Sordariomycetes), the reference S strain lacks recombination across a 0.8 Mb region around the mating-type locus. The lack of recombination in this region ensures that nuclei of opposite mating types are packaged into a single ascospore (pseudo-homothallic lifecycle). We found evidence for a lack of recombination around the mating-type locus in the genomes of 10 P. anserina strains and six closely related pseudo-homothallic Podospora species. Importantly, the size of the non-recombining region differed between strains and species, as indicated by the heterozygosity levels around the mating-type locus and experimental selfing. The non-recombining region is probably labile and polymorphic, differing in size and precise location within and between species, resulting in occasional, but infrequent, recombination at a given base pair. This view is also supported by the low divergence between mating types, and the lack of strong linkage disequilibrium, chromosomal rearrangements, trans-specific polymorphism and genomic degeneration. We found a pattern suggestive of evolutionary strata in P. pseudocomata. The observed heterozygosity levels indicate low but non-null outcrossing rates in nature in these pseudo-homothallic fungi. This study adds to our understanding of mating-type chromosome evolution and its relationship to mating systems.

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Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom Agaricus bisporus

Genes ◽

10.3390/genes12071079 ◽

2021 ◽

Vol 12 (7) ◽

pp. 1079

Author(s):

Marie Foulongne-Oriol ◽

Ozgur Taskent ◽

Ursula Kües ◽

Anton S. M. Sonnenberg ◽

Arend F. van Peer ◽

...

Keyword(s):

Mating Type ◽

Agaricus Bisporus ◽

Reference Genome ◽

Mating Types ◽

Button Mushroom ◽

Recombination Suppression ◽

Type Locus ◽

Mating Type Locus ◽

Sexual Compatibility ◽

Single Mating

In heterothallic basidiomycete fungi, sexual compatibility is restricted by mating types, typically controlled by two loci: PR, encoding pheromone precursors and pheromone receptors, and HD, encoding two types of homeodomain transcription factors. We analysed the single mating-type locus of the commercial button mushroom variety, Agaricus bisporus var. bisporus, and of the related variety burnettii. We identified the location of the mating-type locus using genetic map and genome information, corresponding to the HD locus, the PR locus having lost its mating-type role. We found the mip1 and β-fg genes flanking the HD genes as in several Agaricomycetes, two copies of the β-fg gene, an additional HD2 copy in the reference genome of A. bisporus var. bisporus and an additional HD1 copy in the reference genome of A. bisporus var. burnettii. We detected a 140 kb-long inversion between mating types in an A. bisporus var. burnettii heterokaryon, trapping the HD genes, the mip1 gene and fragments of additional genes. The two varieties had islands of transposable elements at the mating-type locus, spanning 35 kb in the A. bisporus var. burnettii reference genome. Linkage analyses showed a region with low recombination in the mating-type locus region in the A. bisporus var. burnettii variety. We found high differentiation between β-fg alleles in both varieties, indicating an ancient event of recombination suppression, followed more recently by a suppression of recombination at the mip1 gene through the inversion in A. bisporus var. burnettii and a suppression of recombination across whole chromosomes in A. bisporus var. bisporus, constituting stepwise recombination suppression as in many other mating-type chromosomes and sex chromosomes.

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