Tempo of degeneration across independently evolved non-recombining regions

Abstract

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.

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

“…tatarinowii (Fig. 1; Carpentier et al 2021), which suggests an independent evolution in this later lineage. We did not find on M. v. parryi footprints of the light blue stratum previously identified in M. v. caroliniana (Branco et al 2018) 4 and Supplementary Table S5).…”

“…The different genes within each locus have been linked since the emergence of the basidiomycete clade (Coelho et al, 2017;Sun et al, 2019), and recombination suppression extended in the local region around each of the two matingtype loci early in the diversification of Microbotryum fungi, generating independent evolutionary strata around the PR locus (called purple stratum) and HD locus (called blue stratum), and later another stratum (called orange) distal to the purple stratum (Branco et al, 2017). Subsequently, at least eight independent events of recombination suppression involving different chromosomal rearrangements linked the HD and PR loci (Branco et al, 2018;Carpentier et al, 2021). The linkage of PR to HD mating-type determining genes is beneficial under the highly selfing system of Microbotryum fungi; only two mating types are then produced by a diploid individual, leading to a 1/2 compatibility among gametes under inter-tetrad selfing, i.e.…”

Dynamics of transposable element accumulation in the non-recombining regions of mating-type chromosomes in anther-smut fungi

“…TE density was generally higher in older evolutionary strata such as the purple stratum (Supplementary Figure S7H, S7J and S7O) and lower in young strata such as the young pink and white strata of M. v. paradoxa (Supplementary Figure S7G). In part because of this variation in TE content, the size of the mating-type chromosomes varied greatly across Microbotryum species (Figure 1B), from 1,177,022 bp in M. scabiosae to 10,060,889 bp in M. v. paradoxa (3,076,521 bp on average); the size of the mating-type chromosomes also varies because different chromosomal rearrangements were at the origin of HD-PR locus linkage (Duhamel et al, 2022). For the same reasons, the size of the non-recombining regions was variable, ranging from 630,774 bp in M. scabiosae to 9,461,162 bp in M. v. paradoxa, thus spanning almost the full length of the mating-type chromosome in this later species (Figure 1B), and being absent in M. intermedium.…”

“…Fungal mating-type chromosomes are similarly useful models and share key features with sex chromosomes: they can display large non-recombining regions, with evolutionary strata of different ages as well as footprints of degeneration (Menkis et al ., 2008; Whittle et al ., 2011; Fontanillas et al ., 2015; Idnurm et al ., 2015; Branco et al ., 2018; Hartmann et al ., 2021; Carpentier et al ., 2022). When they occur, the non-recombining regions on fungal mating-type chromosomes are relatively young and some genera display multiple independent events of recombination cessation across closely related species, allowing to study the early stages of genomic degenerescence with independent data points (Carpentier et al ., 2022). In addition, fungi generally have small genomes and can be cultivated at the haploid phase, facilitating genomic assemblies and comparisons.…”

Domestication of different varieties in the cheese-making fungusGeotrichum candidum

“…This was the case even in the clonal Cheese_2 population, while degeneration can be expected to be particularly strong in clonally replicated populations as recombination allows more efficient selection. The absence of sexual reproduction in the Cheese_2 population may be too recent to observe degeneration (Carpentier et al, 2022). We also investigated the presence of premature stop codons due to nonsense mutations in all genes with predicted functions in both CLIB 918 and LMA-244 reference genomes.…”