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

2017 ◽  
Vol 114 (27) ◽  
pp. 7067-7072 ◽  
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.

scholarly journals Differential Gene Expression between Fungal Mating Types Is Associated with Sequence Degeneration

2020 ◽  
Vol 12 (4) ◽  
pp. 243-258 ◽  
Author(s):  
Wen-Juan Ma ◽  
Fantin Carpentier ◽  
Tatiana Giraud ◽  
Michael E Hood
Keyword(s):  
Differential Expression ◽  
Differentially Expressed Genes ◽  
Mating Type ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Gc Content ◽  
Differentially Expressed ◽  
Mating Types ◽  
Sexual Antagonism ◽  
Recombination Suppression

Abstract Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.

scholarly journals Corrigendum: Convergent recombination cessation between mating-type genes and centromeres in selfing anther-smut fungi

2020 ◽  
Vol 30 (3) ◽  
pp. 514-514
Author(s):  
Fantin Carpentier ◽  
Ricardo C. Rodríguez de la Vega ◽  
Sara Branco ◽  
Alodie Snirc ◽  
Marco A. Coelho ◽  
...  
Keyword(s):  
Mating Type ◽  
Smut Fungi ◽  
Anther Smut ◽  
Mating Type Genes

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

2021 ◽  
Author(s):  
Marine Duhamel ◽  
Fantin Carpentier ◽  
Dominik Begerow ◽  
Michael Hood ◽  
Ricardo C Rodriguez de la Vega ◽  
...  
Keyword(s):  
Mating Type ◽  
Chromosomal Rearrangements ◽  
Smut Fungi ◽  
Recombination Suppression ◽  
Type Locus ◽  
Genomic Changes ◽  
Mating Type Locus ◽  
Independent Events ◽  
Anther Smut ◽  
Genomic Regions

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.

scholarly journals Convergent recombination cessation between mating-type genes and centromeres in selfing anther-smut fungi

2019 ◽  
Vol 29 (6) ◽  
pp. 944-953 ◽  
Author(s):  
Fantin Carpentier ◽  
Ricardo C. Rodríguez de la Vega ◽  
Sara Branco ◽  
Alodie Snirc ◽  
Marco A. Coelho ◽  
...  
Keyword(s):  
Mating Type ◽  
Smut Fungi ◽  
Anther Smut ◽  
Mating Type Genes

scholarly journals Deletion of the Schizophyllum commune Aα Locus: The Roles of Aα Y and Z Mating-Type Genes

Genetics ◽  
1996 ◽  
Vol 144 (4) ◽  
pp. 1437-1444
Author(s):  
C Ian Robertson ◽  
Kirk A Bartholomew ◽  
Charles P Novotny ◽  
Robert C Ullrich
Keyword(s):  
Mating Type ◽  
Sexual Development ◽  
Schizophyllum Commune ◽  
Mating Types ◽  
Developmental Pathway ◽  
Mating Type Gene ◽  
Mating Type Genes ◽  
Regulatory Loci ◽  
Type Gene

The Aα locus is one of four master regulatory loci that determine mating type and regulate sexual development in Schizophyllum commune. We have made a plasmid containing a URA1 gene disruption of the Aα Y1 gene. Y1 is the sole Aα gene in Aα1 strains. We used the plasmid construction to produce an Aα null (i.e., AαΔ) strain by replacing the genomic Y1 gene with URA1 in an Aα1 strain. To characterize the role of the Aα genes in the regulation of sexual development, we transformed various Aα Y and Z alleles into AαΔ strains and examined the acquired mating types and mating abilities of the transformants. These experiments demonstrate that the Aα Y gene is not essential for fungal viability and growth, that a solitary Z Aα mating-type gene does not itself activate development, that Aβ proteins are sufficient to activate the A developmental pathway in the absence of Aα proteins and confirm that Y and Z genes are the sole determinants of Aα mating type. The data from these experiments support and refine our model of the regulation of A-pathway events by Y and Z proteins.

The origin of multiple mating types in mushrooms

1993 ◽  
Vol 104 (2) ◽  
pp. 227-230
Author(s):  
U. Kues ◽  
L.A. Casselton
Keyword(s):  
Mating Type ◽  
Multiple Mating ◽  
Mating Types ◽  
Mating Partner ◽  
Binucleate Cells ◽  
Large Numbers ◽  
Mating Type Genes ◽  
And Function ◽  
Developmental Switch ◽  
Sterile Mycelium

Having multiple mating types greatly improves the chances of meeting a compatible mating partner, particularly in an organism like the mushroom that has no sexual differentiation and no mechanism for signalling to a likely mate. Having several thousands of mating types, as some mushrooms do, is, however, remarkable - and even more remarkable is the fact that individuals only recognise that they have met a compatible mate after their cells have fused. How are such large numbers of mating types generated and what is the nature of the intracellular interaction that distinguishes self from non- self? Answers to these fascinating questions come from cloning some of the mating type genes of the ink cap mushroom Coprinus cinereus. A successful mating in Coprinus triggers a major switch in cell type, the conversion of a sterile mycelium with uninucleate cells (monokaryon) to a fertile mycelium with binucleate cells (dikaryon) which differentiates the characteristic fruit bodies. The mating type genes that regulate this developmental switch map to two multiallelic loci designated A and B and these must both carry different alleles for full mating compatibility. A and B independently regulate different steps in the developmental switch, making it possible to study just one component of the system and work in our laboratory has concentrated on understanding the structure and function of the A genes. It is estimated that some 160 different A mating types exist in nature, any two of which can together trigger the A-regulated part of sexual development. The first clue to how such large numbers are generated came from classical genetic analysis, which identified two functionally redundant A loci, (alpha) and beta. Functional redundancy is, indeed, the key to multiple A mating types and, as seen in Fig.1, molecular cloning has identified many more genes than was possible by recombination analysis.

Evidence for mitochondrial gene control of mating types in Phytophthora

2005 ◽  
Vol 51 (11) ◽  
pp. 934-940 ◽  
Author(s):  
Yu-Huan Gu ◽  
Wen-Hsiung Ko
Keyword(s):  
Mating Type ◽  
Mitochondrial Gene ◽  
Phytophthora Capsici ◽  
Nuclear Genes ◽  
Gene Control ◽  
Mating Types ◽  
Phytophthora Parasitica ◽  
Decisive Effect ◽  
Mating Type Genes ◽  
Fusion Products

When protoplasts carrying metalaxyl-resistant (Mr) nuclei from the A1 isolate of Phytophthora parasitica were fused with protoplasts carrying chloroneb-resistant (Cnr) nuclei from the A2 isolate of the same species, fusion products carrying Mr nuclei were either the A2 or A1A2 type, while those carrying Cnr nuclei were the A1, A2, or A1A2 type. Fusion products carrying Mr and Cnr nuclei also behaved as the A1, A2, or A1A2 type. The result refutes the hypothesis that mating types in Phytophthora are controlled by nuclear genes. When nuclei from the A1 isolate of P. parasitica were fused with protoplasts from the A2 isolate of the same species and vice versa, all of the nuclear hybrids expressed the mating type characteristics of the protoplast parent. The same was true when the nuclei from the A1 isolate of P. parasitica were fused with the protoplasts from the A0 isolate of Phytophthora capsici and vice versa. These results confirm the observation that mating type genes are not located in the nuclei and suggest the presence of mating type genes in the cytoplasms of the recipient protoplasts. When mitochondria from the A1 isolate of P. parasitica were fused with protoplasts from the A2 isolate of the same species, the mating type of three out of five regenerated protoplasts was changed to the A1 type. The result demonstrated the decisive effect of mitochondrial donor sexuality on mating type characteristics of mitochondrial hybrids and suggested the presence of mating type genes in mitochondria. All of the mitochondrial hybrids resulting from the transfer of mitochondria from the A0 isolate of P. capsici into protoplasts from the A1 isolate of P. parasitica were all of the A0 type. The result supports the hypothesis of the presence of mating type genes in mitochondria in Phytophthora.Key words: mating type, mitochondrial gene, Phytophthora parasitica, Phytophthora capsici.

scholarly journals Degeneration in Codon Usage within the Region of Suppressed Recombination in the Mating-Type Chromosomes of Neurospora tetrasperma

2011 ◽  
Vol 10 (4) ◽  
pp. 594-603 ◽  
Author(s):  
C. A. Whittle ◽  
Y. Sun ◽  
H. Johannesson
Keyword(s):  
Codon Usage ◽  
Mating Type ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sex Chromosome Evolution ◽  
Recombination Suppression ◽  
Content Type ◽  
Genomic Changes ◽  
Suppressed Recombination ◽  
Neurospora Tetrasperma

ABSTRACT The origin and early evolution of sex chromosomes are currently poorly understood. The Neurospora tetrasperma mating-type ( mat ) chromosomes have recently emerged as a model system for the study of early sex chromosome evolution, since they contain a young (<6 million years ago [Mya]), large (>6.6-Mb) region of suppressed recombination. Here we examined preferred-codon usage in 290 genes (121,831 codon positions) in order to test for early signs of genomic degeneration in N. tetrasperma mat chromosomes. We report several key findings about codon usage in the region of recombination suppression, including the following: (i) this region has been subjected to marked and largely independent degeneration among gene alleles; (ii) the level of degeneration is magnified over longer periods of recombination suppression; and (iii) both mat a and mat A chromosomes have been subjected to deterioration. The frequency of shifts from preferred codons to nonpreferred codons is greater for shorter genes than for longer genes, suggesting that short genes play an especially significant role in early sex chromosome evolution. Furthermore, we show that these degenerative changes in codon usage are best explained by altered selection efficiency in the recombinationally suppressed region. These findings demonstrate that the fungus N. tetrasperma provides an effective system for the study of degenerative genomic changes in young regions of recombination suppression in sex-regulating chromosomes.

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

2019 ◽  
Vol 37 (3) ◽  
pp. 668-682 ◽  
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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