scholarly journals Sex-linked transcriptional divergence in the hermaphrodite fungus Neurospora tetrasperma

2013 ◽  
Vol 280 (1764) ◽  
pp. 20130862 ◽  
Author(s):  
Nicklas Samils ◽  
Anastasia Gioti ◽  
Magnus Karlsson ◽  
Yu Sun ◽  
Takao Kasuga ◽  
...  
Keyword(s):  
Mating Type ◽  
Sequence Divergence ◽  
Differentially Expressed ◽  
Female Development ◽  
Molecular Phenotype ◽  
Filamentous Ascomycete ◽  
Agar Media ◽  
Suppressed Recombination ◽  
Neurospora Tetrasperma ◽  
Male Tissue

In the filamentous ascomycete Neurospora tetrasperma , a large (approx. 7 Mbp) region of suppressed recombination surrounds the mating-type ( mat ) locus. While the remainder of the genome is largely homoallelic, this region of recombinational suppression, extending over 1500 genes, is associated with sequence divergence. Here, we used microarrays to examine how the molecular phenotype of gene expression level is linked to this divergent region, and thus to the mating type. Culturing N. tetrasperma on agar media that induce sexual/female or vegetative/male tissue, we found 196 genes significantly differentially expressed between mat A and mat a mating types. Our data show that the genes exhibiting mat -linked expression are enriched in the region genetically linked to mating type, and sequence and expression divergence are positively correlated. Our results indicate that the phenotype of mat A strains is optimized for traits promoting sexual/female development and the phenotype of mat a strains for vegetative/male development. This discovery of differentially expressed genes associated with mating type provides a link between genotypic and phenotypic divergence in this taxon and illustrates a fungal analogue to sexual dimorphism found among animals and plants.

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 Pseudohomothallism and Evolution of the Mating-Type Chromosome in Neurospora tetrasperma

Genetics ◽  
1996 ◽  
Vol 143 (2) ◽  
pp. 789-799 ◽  
Author(s):  
Sandra T Merino ◽  
Mary Anne Nelson ◽  
David J Jacobson ◽  
Donald O Natvig
Keyword(s):  
Genetic Variability ◽  
Mating Type ◽  
High Frequency ◽  
Population Biology ◽  
Unexpected Result ◽  
Evolutionary Time ◽  
Distinct Haplotype ◽  
Suppressed Recombination ◽  
Neurospora Tetrasperma ◽  
Type Chromosome

Abstract Ascospores of Neurospora tetrasperma normally contain nuclei of both mating-type idiomorphs (a and A), resulting in self-fertile heterokaryons (a type of sexual reproduction termed pseudohomothallism). Occasional homokaryotic self-sterile strains (either a or A) behave as heterothallics and, in principle, provide N. tetrasperma with a means for facultative outcrossing. This studywas conceived as an investigation of the population biology of N. tetrasperma to assess levels of intrastrain heterokaryosis (heterozygosity). The unexpected result was that the mating-type chromosome and autosomes exhibited very different patterns of evolution, apparently because of suppressed recombination between mating-type chromosomes. Analysis of sequences on the mating-type chromosomes of wild-collected self-fertile strains revealed high levels of genetic variability between sibling A and a nuclei. In contrast, sequences on autosomes of sibling A and a nuclei exhibited nearly complete homogeneity. Conservation of distinct haplotype combinations on A and a mating-type chromosomes in strains from diverse locations further suggested an absence of recombination over substantial periods of evolutionary time. The suppression of recombination on the N. tetrasperma mating-type chromosome, expected to ensure a high frequency of self fertility, presents an interesting parallel with, and possible model for studying aspects of, the evolution of mammalian sex chromosomes.

scholarly journals Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma

PLoS Genetics ◽  
2012 ◽  
Vol 8 (7) ◽  
pp. e1002820 ◽  
Author(s):  
Yu Sun ◽  
Pádraic Corcoran ◽  
Audrius Menkis ◽  
Carrie A. Whittle ◽  
Siv G. E. Andersson ◽  
...  
Keyword(s):  
Mating Type ◽  
Large Scale ◽  
Filamentous Ascomycete ◽  
Neurospora Tetrasperma

scholarly journals Suppressed Recombination and a Pairing Anomaly on the Mating-Type Chromosome of Neurospora tetrasperma

Genetics ◽  
2000 ◽  
Vol 154 (2) ◽  
pp. 623-633 ◽  
Author(s):  
Alena Gallegos ◽  
David J Jacobson ◽  
Namboori B Raju ◽  
Marian P Skupski ◽  
Donald O Natvig
Keyword(s):  
Mating Type ◽  
Mitotic Division ◽  
Crossing Over ◽  
Unpaired Region ◽  
Wild Strains ◽  
Suppressed Recombination ◽  
Pseudoautosomal Regions ◽  
Neurospora Tetrasperma ◽  
Type Chromosome ◽  
Chromosome Disjunction

Abstract Neurospora crassa and related heterothallic ascomycetes produce eight homokaryotic self-sterile ascospores per ascus. In contrast, asci of N. tetrasperma contain four self-fertile ascospores each with nuclei of both mating types (matA and mata). The self-fertile ascospores of N. tetrasperma result from first-division segregation of mating type and nuclear spindle overlap at the second meiotic division and at a subsequent mitotic division. Recently, Merino et al. presented population-genetic evidence that crossing over is suppressed on the mating-type chromosome of N. tetrasperma, thereby preventing second-division segregation of mating type and the formation of self-sterile ascospores. The present study experimentally confirmed suppressed crossing over for a large segment of the mating-type chromosome by examining segregation of markers in crosses of wild strains. Surprisingly, our study also revealed a region on the far left arm where recombination is obligatory. In cytological studies, we demonstrated that suppressed recombination correlates with an extensive unpaired region at pachytene. Taken together, these results suggest an unpaired region adjacent to one or more paired regions, analogous to the nonpairing and pseudoautosomal regions of animal sex chromosomes. The observed pairing and obligate crossover likely reflect mechanisms to ensure chromosome disjunction.

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 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 Unique Patterns of Mating Pheromone Presence and Absence could Result in the Ambiguous Sexual Behaviours of Colletotrichum Species

2020 ◽  
Author(s):  
Andrea Melissa Wilson ◽  
RV Lelwala ◽  
PWJ Taylor ◽  
MJ Wingfield ◽  
BD WINGFIELD
Keyword(s):  
Mating Type ◽  
Molecular Mechanisms ◽  
Mating Strategies ◽  
Mating Partner ◽  
Filamentous Ascomycete ◽  
Sexual Behaviours ◽  
History Of ◽  
Ascomycete Fungi ◽  
Presence And Absence ◽  
Sexual Progeny

Abstract Background: Colletotrichum species are known to engage in unique sexual behaviours that differ significantly from the mating strategies of other filamentous ascomycete species. Most ascomycete fungi require the expression of both the MAT1-1-1 and MAT1-2-1 genes to regulate mating type and induce sexual reproduction. In contrast, all isolates of Colletotrichum are known to harbour only the MAT1-2-1 gene and yet, are capable of recognizing suitable mating partners and producing sexual progeny. The molecular mechanisms contributing to mating types and behaviours in Colletotrichum are thus unknown. Results: A comparative genomics approach analysing genomes from 47 Colletotrichum isolates was used to elucidate a putative molecular mechanism underlying the unique sexual behaviours observed in Colletotrichum species. The existence of only the MAT1-2 idiomorph was confirmed across all species included in this study. Comparisons at the loci harbouring the two mating pheromones and their cognate receptors revealed interesting patterns of gene presence and absence as well as gene loss. The results also showed that these genes have been lost multiple times over the evolutionary history of this genus. Conclusion: The multiple losses of the pheromone genes in these species suggest strong selection against the typical mating strategies seen in other species. This further suggests that these pheromones no longer play a role in mating type determination and that the species of this genus have undiscovered mechanisms by which to control mating type and mating partner recognition. This research thus provides a base from which further interrogation of this topic can take place.

scholarly journals Gene expression vs. sequence divergence: comparative transcriptome sequencing among natural Rhinolophus ferrumequinum populations with different acoustic phenotypes

2019 ◽  
Vol 16 (1) ◽  
Author(s):  
Hanbo Zhao ◽  
Hui Wang ◽  
Tong Liu ◽  
Sen Liu ◽  
Longru Jin ◽  
...  
Keyword(s):  
Gene Expression ◽  
Geographic Variation ◽  
Molecular Mechanisms ◽  
Sequence Divergence ◽  
Orthologous Gene ◽  
Differentially Expressed ◽  
Nucleotide Polymorphisms ◽  
Genetic Lineages ◽  
Rhinolophus Ferrumequinum ◽  
Horseshoe Bat

Abstract Background Although the sensory drive hypothesis can explain the geographic variation in echolocation frequencies of some bat species, the molecular mechanisms underlying this phenomenon are still unclear. The three lineages of greater horseshoe bat (Rhinolophus ferrumequinum) in China (northeast, central-east, and southwest) have significant geographic variation in resting frequencies (RF) of echolocation calls. Because their cochleae have an acoustic fovea that is highly sensitive to a narrow range of frequencies, we reported the transcriptomes of cochleae collected from three genetic lineages of R. ferrumequinum, which is an ideal organism for studying geographic variation in echolocation signals, and tried to understand the mechanisms behind this bat phenomenon by analyzing gene expression and sequence variation. Results A total of 8190 differentially expressed genes (DEGs) were identified. We identified five modules from all DEGs that were significantly related to RF or forearm length (FL). DEGs in the RF-related modules were significantly enriched in the gene categories involved in neural activity, learning, and response to sound. DEGs in the FL-related modules were significantly enriched in the pathways related to muscle and actin functions. Using 21,945 single nucleotide polymorphisms, we identified 18 candidate unigenes associated with hearing, five of which were differentially expressed among the three populations. Additionally, the gene ERBB4, which regulates diverse cellular processes in the inner ear such as cell proliferation and differentiation, was in the largest module. We also found 49 unigenes that were under positive selection from 4105 one-to-one orthologous gene pairs between the three R. ferrumequinum lineages and three other Chiroptera species. Conclusions The variability of gene expression and sequence divergence at the molecular level might provide evidence that can help elucidate the genetic basis of geographic variation in echolocation signals of greater horseshoe bats.

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