Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation

Abstract

The rate of meiotic crossing over (CO) varies considerably along chromosomes, leading to marked distortions between physical and genetic distances. The causes underlying this variation are being unraveled, and DNA sequence and chromatin states have emerged as key factors. However, the extent to which the suppression of COs within the repeat-rich pericentromeric regions of plant and mammalian chromosomes results from their high level of DNA polymorphisms and from their heterochromatic state, notably their dense DNA methylation, remains unknown. Here, we test the combined effect of removing sequence polymorphisms and repeat-associated DNA methylation on the meiotic recombination landscape of an Arabidopsis mapping population. To do so, we use genome-wide DNA methylation data from a large panel of isogenic epigenetic recombinant inbred lines (epiRILs) to derive a recombination map based on 126 meiotically stable, differentially methylated regions covering 81.9% of the genome. We demonstrate that the suppression of COs within pericentromeric regions of chromosomes persists in this experimental setting. Moreover, suppression is reinforced within 3-Mb regions flanking pericentromeric boundaries, and this effect appears to be compensated by increased recombination activity in chromosome arms. A direct comparison with 17 classical Arabidopsis crosses shows that these recombination changes place the epiRILs at the boundary of the range of natural variation but are not severe enough to transgress that boundary significantly. This level of robustness is remarkable, considering that this population represents an extreme with key recombination barriers having been forced to a minimum.eiotic recombination is a fundamental process in genetics whereby maternally and paternally inherited homologous chromosomes exchange material, either nonreciprocally by gene conversion or reciprocally by crossing over (CO). COs are not distributed uniformly along the genome but occur more often in chromosome arms and are strongly suppressed in pericentromeric regions (1-3), partly as a result of sequence and chromatin determinants (1,(4)(5)(6)(7)(8). It is commonly believed that in plants and mammals high levels of DNA sequence polymorphisms as well as heterochromatic features associated with repeats, notably dense DNA methylation and transcriptional silencing, play a central role in this suppression (1, 4).Suppression of COs by dense DNA methylation has been demonstrated experimentally in the fungus Ascobolus (7). Specifically, COs were reduced when the recombination interval was methylated on one homolog and were abolished almost completely when methylated on both homologs. In Arabidopsis, two recent mapping studies analyzed F 2 progeny derived from crosses between Columbia ddm1 and met1 [Col(ddm1),Col(met1)] DNA methylation mutants and wild-type Landsberg [Ler(WT)] accessions and showed that loss of DNA methylation could not alleviate the suppression of COs in pericentromeric regions of chromosomes (9, 10). However, as pointed out by the aut...

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

“…DNA methylation also represses CO formation (Maloisel and Rossignol 1998) and is sufficient to silence CO hotspots in Arabidopsis (Yelina et al 2015). CO distribution is largely modified in Arabidopsis met1 and ddm1 mutants, which show an increase of proximal recombination events and a simultaneous decrease in pericentromeric and distal regions (Colome-Tatche et al 2012;Melamed-Bessudo and Levy 2012;Mirouze et al 2012;Yelina et al 2012). Since H3K4me3 and H2A.Z landmarks are important for promotion of gene transcription (Liu et al 2009;Yelina et al 2012;Choi et al 2013) and are associated with high recombination rates in Arabidopsis (Yelina et al 2012) as well as in barley (Aliyeva-Schnorr et al 2015;Baker et al 2015), this suggests that both recombination and DNA-transposon insertion benefit from low compaction of DNA to occur within the genome.…”

Epigenetic diversity increases the productivity and stability of plant populations

“…After a backcross of the F1 with the wild type, inbred lines were established from F2 plants homozygous at DDM1, which were thus nearly identical in DNA sequence, but, through recombination, differed greatly in their patterns of DNA methylation. Using stringent criteria, 2611 differentially methylated regions (DMRs) could be identified between the two parental lines, of which approximately one-third were stably inherited for at least eight generations 28 . Recent data show that these DMRs are even stable for over 16 generations in the epiRIL population (Table 4).…”

“…We achieved this by working with epigenetic recombinant inbred lines (epiRILs) of Arabidopsis thaliana, lines that were derived from two parents with near identical genome sequence but highly contrasted DNA methylation profiles 25 . Previous research has shown that these epiRILs are highly variable in DNA methylation and represent a mosaic of their parents' epigenomes, and that a large fraction of the DNA methylation differences among epiRILs are stably inherited for many generations 28 . Starting from a pool of 20 epiRILs, we created monocultures of each epiRIL, as well as populations composed of 2, 4 or 16 epiRILs, respectively, and we subjected these populations to a factorial combination of pathogen attack and weed competition.…”

Comprehensive gene expression analysis of the DNA (cytosine-5) methyltransferase family in rice (Oryza sativa L.)

“…In plants, specific DNA MTases (MET1, DRM, and CMT) are essential for the creation of such patterns. Altered patterns of DNA methylation (as observed in ddm1 or met1 mutants) can be transmissible in many generations, even following backcrossing to wild-type plants (Reinders et al, 2009;Colomé-Tatché et al, 2012). Meanwhile, genes of different DNA MTases are expressed differentially under different conditions.…”