Epigenomic and structural events preclude recombination in Brassica napus

Abstract

Meiotic recombination is a major evolutionary process generating genetic diversity at each generation in sexual organisms. However, this process is highly regulated, with the majority of crossovers lying in the distal chromosomal regions that harbor low DNA methylation levels. Even in these regions, some islands without recombination remain, for which we investigated the underlying causes.Genetic maps were established in two Brassica napus hybrids to detect the presence of such large nonrecombinant islands. The role played by DNA methylation and structural variations in this local absence of recombination was determined by performing bisulfite sequencing and whole genome comparisons. Inferred structural variations were validated using either optical mapping or oligo fluorescence in situ hybridization.Hypermethylated or inverted regions between Brassica genomes were associated with the absence of recombination. Pairwise comparisons of nine B. napus genome assemblies revealed that such inversions occur frequently and may contain key agronomic genes such as resistance to biotic stresses.We conclude that such islands without recombination can have different origins, such as DNA methylation or structural variations in B. napus. It is thus essential to take into account these features in breeding programs as they may hamper the efficient combination of favorable alleles in elite varieties.

Modeling the stepwise extension of recombination suppression on sex chromosomes and other supergenes through deleterious mutation sheltering

“…Our model can thus account for the existence of inversions very close, but not fully linked to a mating-type locus, as reported in the chestnut blast fungus (41,42). Similar results were also obtained when we considered recombination modifiers suppressing recombination even when homozygous, as for histone modifications or methylation (43), rather than solely when heterozygous, as for inversions (Figure S14). Similar results were also observed if we assumed that the fitness effects of mutations occurring across the genome were drawn from a gamma distribution (i.e.…”

“…We did not include possible decreases in fertility due to segregation issues arising during meiosis as a result of inversions in our model ( 49 ); such issues would, clearly, decrease the probability of inversion fixation as a function of the fitness cost, as for any other model explaining the evolution of the stepwise extension of recombination suppression involving inversions. However, our model holds for any mechanism of recombination suppression (it is not limited to inversions) and the other possible mechanisms [such as methylation ( 43 )] would not be expected to decrease fertility. Given the lack of knowledge about inversion rates in natural conditions and the computation challenge represented by the simulation of complex patterns of recombination, we used reasonably high inversion rates in our sexchromosome evolution simulations, making it possible to observe the stepwise extension of a nonrecombining region within 100,000 generations.…”

Sheltering of deleterious mutations explains the stepwise extension of recombination suppression on sex chromosomes and other supergenes

“…Similar results were obtained when: (i) 2 or more permanently heterozygous alleles segregated at a mating incompatibility locus, modeling plant self-incompatibility or fungal mating-type systems ( S5 and S14 Figs; [ 5 , 42 ]); (ii) the alleles were not permanently heterozygous, but were strongly overdominant, thus occurring mostly in the heterozygous state, as for several supergenes controlling color polymorphism ( S8 Fig ; [ 13 , 43 , 44 ]); (iii) the fitness effects of mutations occurring across the genome were drawn from a gamma distribution (i.e., the mutations segregating in populations had different fitness effects; S17 Fig ); (iv) recombination modifiers suppressed recombination even when homozygous, as for histone modifications or methylation [ 45 ], rather than solely when heterozygous, as for inversions ( S14 Fig ); and (v) the inversion was in strong but incomplete linkage with the permanently heterozygous allele (e.g., 0.1 cM away from the allele, S4 to S8 Figs). Our model can thus account for the existence of inversions very close, but not fully linked to a mating-type locus, as reported in the chestnut blast fungus [ 46 , 47 ].…”

Integrating Genetic and Chromosome Maps of Allium Cepa: From Markers Visualization to Genome Assembly Verification

“…Moreover, the detection of methylated chromosome regions with antibodies to 5-mC showed that subtelomeric region bearing satellite DNA are always methylated and next to it region of highly repeated DNA are often methylated in short arm of chromosome 2 of A. cepa [42]. Hypermethylated region is associated with the absence of recombination [43] and is sufficient to silence crossover hot spots [44]. Thus, the discrepancy between the order of the location of markers on the genetic map and the physical chromosome is most likely associated with the suppression of recombination in this region of the chromosome.…”