scholarly journals Tempo of degeneration across independently evolved non-recombining regions

2021 ◽  
Author(s):  
Fantin Carpentier ◽  
Ricardo Rodriguez De La Vega ◽  
Michael H. Perlin ◽  
Margaret Wallen ◽  
Michael Hood ◽  
...  
Keyword(s):  
Codon Usage ◽  
Gene Conversion ◽  
Mating Type ◽  
Genetic Diseases ◽  
Smut Fungi ◽  
Recombination Suppression ◽  
Optimal Codons ◽  
Optimal Codon ◽  
Biased Gene Conversion

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.

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 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 Codon Usage Bias in Animals: Disentangling the Effects of Natural Selection, Effective Population Size, and GC-Biased Gene Conversion

2018 ◽  
Vol 35 (5) ◽  
pp. 1092-1103 ◽  
Author(s):  
Nicolas Galtier ◽  
Camille Roux ◽  
Marjolaine Rousselle ◽  
Jonathan Romiguier ◽  
Emeric Figuet ◽  
...  
Keyword(s):  
Natural Selection ◽  
Codon Usage ◽  
Population Size ◽  
Gene Conversion ◽  
Effective Population Size ◽  
Codon Usage Bias ◽  
Effective Population ◽  
Biased Gene Conversion

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

2019 ◽  
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.

scholarly journals Biased gene conversion drives codon usage in human and precludes selection on translation efficiency

2016 ◽  
Author(s):  
Fanny Pouyet ◽  
Dominique Mouchiroud ◽  
Laurent Duret ◽  
Marie Sémon
Keyword(s):  
Gene Expression ◽  
Codon Usage ◽  
Gene Conversion ◽  
Large Scale ◽  
Synonymous Codon ◽  
Gc Content ◽  
Intragenic Recombination ◽  
Translation Efficiency ◽  
Functional Categories ◽  
Biased Gene Conversion

AbstractIn humans, as in other mammals, synonymous codon usage (SCU) varies widely among genes. In particular, genes involved in cell differentiation or in proliferation display a distinct codon usage, suggesting that SCU is adaptively constrained to optimize translation efficiency in distinct cellular states. However, in mammals, SCU is known to correlate with large-scale fluctuations of GC-content along chromosomes, caused by meiotic recombination, via the non-adaptive process of GC-biased gene conversion (gBGC). To disentangle and to quantify the different factors driving SCU in humans, we analyzed the relationships between functional categories, base composition, recombination, and gene expression. We first demonstrate that SCU is predominantly driven by large-scale variation in GC-content and is not linked to constraints on tRNA abundance, which excludes an effect of translational selection. In agreement with the gBGC model, we show that differences in SCU among functional categories are explained by variation in intragenic recombination rate, which, in turn, is strongly negatively correlated to gene expression levels during meiosis. Our results indicate that variation in SCU among functional categories (including variation associated to differentiation or proliferation) result from differences in levels of meiotic transcription, which interferes with the formation of crossovers and thereby affects gBGC intensity within genes. Overall, the gBGC model explains 70% of the variance in SCU among genes. We argue that the strong heterogeneity of SCU induced by gBGC in mammalian genomes precludes any optimization of the tRNA pool to the demand in codon usage.

scholarly journals Forces that influence the evolution of codon bias

2010 ◽  
Vol 365 (1544) ◽  
pp. 1203-1212 ◽  
Author(s):  
Paul M. Sharp ◽  
Laura R. Emery ◽  
Kai Zeng
Keyword(s):  
Codon Usage ◽  
Translational Efficiency ◽  
Bacterial Growth Rate ◽  
Frequency Spectra ◽  
Synonymous Codons ◽  
Optimal Codons ◽  
Highly Expressed Genes ◽  
Low Levels ◽  
Highly Correlated

The frequencies of alternative synonymous codons vary both among species and among genes from the same genome. These patterns have been inferred to reflect the action of natural selection. Here we evaluate this in bacteria. While intragenomic variation in many species is consistent with selection favouring translationally optimal codons, much of the variation among species appears to be due to biased patterns of mutation. The strength of selection on codon usage can be estimated by two different approaches. First, the extent of bias in favour of translationally optimal codons in highly expressed genes, compared to that in genes where selection is weak, reveals the long-term effectiveness of selection. Here we show that the strength of selected codon usage bias is highly correlated with bacterial growth rate, suggesting that selection has favoured translational efficiency. Second, the pattern of bias towards optimal codons at polymorphic sites reveals the ongoing action of selection. Using this approach we obtained results that were completely consistent with the first method; importantly, the frequency spectra of optimal codons at polymorphic sites were similar to those predicted under an equilibrium model. Highly expressed genes in Escherichia coli appear to be under continuing strong selection, whereas selection is very weak in genes expressed at low levels.

scholarly journals Codon usage bias in animals: disentangling the effects of natural selection, effective population size and GC-biased gene conversion

2017 ◽  
Author(s):  
N. Galtier ◽  
C. Roux ◽  
M. Rousselle ◽  
J. Romiguier ◽  
E. Figuet ◽  
...  
Keyword(s):  
Natural Selection ◽  
Codon Usage ◽  
Population Size ◽  
Gene Conversion ◽  
Effective Population Size ◽  
Codon Usage Bias ◽  
Effective Population ◽  
Translational Selection ◽  
Wide Range ◽  
Biased Gene Conversion

AbstractSelection on codon usage bias is well documented in a number of microorganisms. Whether codon usage is also generally shaped by natural selection in large organisms, despite their relatively small effective population size (Ne), is unclear. Codon usage bias in animals has only been studied in a handful of model organisms so far, and can be affected by confounding, non-adaptive processes such as GC-biased gene conversion and experimental artefacts. Using population transcriptomics data we analysed the relationship between codon usage, gene expression, allele frequency distribution and recombination rate in 31 non-model species of animals, each from a different family, covering a wide range of effective population sizes. We disentangled the effects of translational selection and GC-biased gene conversion on codon usage by separately analysing GC-conservative and GC-changing mutations. We report evidence for effective translational selection on codon usage in large-Ne species of animals, but not in small-Ne ones, in agreement with the nearly neutral theory of molecular evolution. C- and T-ending codons are generally preferred over synonymous G- and A-ending ones, for reasons that remain to be determined. In contrast, we uncovered a conspicuous effect of GC-biased gene conversion, which is widespread in animals and the main force determining the fate of AT↔GC mutations. Intriguingly, the strength of its effect was uncorrelated with Ne.

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.

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