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

Abstract

Background: Transposable element (TE) activity is generally deleterious to the host fitness, so that genomes often evolve TE control mechanisms, and TE copies are purged by recombination and selection. In the absence of recombination, the number of TE insertions usually increases, but the dynamics of such TE accumulations is unknown. Results: In this study, we investigated the tempo of TE accumulation in the non-recombining genomic regions of 15 Microbotryum species, leveraging on a unique dataset of 21 independent evolutionary strata of recombination cessation of different ages in closely related species. We show that TEs have rapidly accumulated following recombination suppression but that the TE content reached a plateau at ca. 50% of occupied base pairs by 1.5 MY following recombination suppression. The same superfamilies repeatedly expanded in independently evolved non-recombining regions, and in particular Helitrons, despite being scarce before recombination suppression. TEs from the most abundant elements, i.e., Copia and Ty3/Gypsy retrotransposon superfamilies, have also expanded independently in the different non-recombining regions. Copia and Ty3 retrotransposons have accumulated through bursts affecting both the non-recombining regions of the mating-type chromosomes and autosomes at the same time, which supports the TE reservoir hypothesis, i.e., that the TEs accumulated in non-recombining regions have a genome-wide impact by transposing to recombining regions. Conclusion: This study sheds light on the genome-wide consequences of the accumulation of TEs in non-recombining regions, thus improving our knowledge on genome evolution.

Origin and evolutionary trajectories of brown algal sex chromosomes

“…The structural dynamism in the SDR is likely driven by TE-mediated chromosomal rearrangements 44 , since the sex chromosome is enriched in TEs relative to the rest of the genome. As described in other systems, including mating type chromosomes in fungi 45,46 , TE accumulation was likely a consequence of the initial recombination suppression in the SDR 47 which possibly initiated a positive feedback loop between the accumulation of TEs in the sex chromosome and the subsequent rearrangement and expansion of the SDR.…”

Genome biology and evolution of mating type loci in four cereal rust fungi

“…Addressing these knowledge gaps has long been a challenge because initial genome assemblies of rust fungi were fragmented and the structure of the MAT loci could not be assessed consistently. For example, clustering of repetitive elements around MAT loci (17,36,37) is a challenge for studying MAT loci in rust fungi with repeat-rich genomes because repetitive sequences cause gaps, fragmentation, and phase-errors in the assembled genome.…”

An old inversion polymorphism involving giant mobile elements in an invasive fungal pathogen

“…By dating retrotransposon insertions using between-copy divergence and within-copy LTR divergence in both M1400 and M6697 genomes (Fig 5C and D), we found that TEs within the inversion and around the inversion breakpoints were older than TEs farther from the breakpoints. This is expected in non-recombining regions as selection is there less efficient to purge TE insertions so that they remain there longer (Duhamel et al 2023). The date estimates of LTR element insertions (Fig 5D ) further indicated that the TE accumulation in the MAT-proximal region was as old as a few million years, confirming the age estimated based on sequence divergence between MAT-proximal haplotypes.…”