Crossover-active regions of the wheat genome are distinguished by DMC1, the chromosome axis, H3K27me3, and signatures of adaptation

Abstract

The hexaploid bread wheat genome comprises over 16 gigabases of sequence across 21 chromosomes. Meiotic crossovers are highly polarized along the chromosomes, with elevation in the gene-dense distal regions and suppression in the Gypsy retrotransposon-dense centromere-proximal regions. We profiled the genomic landscapes of the meiotic recombinase DMC1 and the chromosome axis protein ASY1 in wheat and investigated their relationships with crossovers, chromatin state, and genetic diversity. DMC1 and ASY1 chromatin immunoprecipitation followed by sequencing (ChIP-seq) revealed strong co-enrichment in the distal, crossover-active regions of the wheat chromosomes. Distal ChIP-seq enrichment is consistent with spatiotemporally biased cytological immunolocalization of DMC1 and ASY1 close to the telomeres during meiotic prophase I. DMC1 and ASY1 ChIP-seq peaks show significant overlap with genes and transposable elements in the Mariner and Mutator superfamilies. However, DMC1 and ASY1 ChIP-seq peaks were detected along the length of each chromosome, including in low-crossover regions. At the fine scale, crossover elevation at DMC1 and ASY1 peaks and genes correlates with enrichment of the Polycomb histone modification H3K27me3. This indicates a role for facultative heterochromatin, coincident with high DMC1 and ASY1, in promoting crossovers in wheat and is reflected in distalized H3K27me3 enrichment observed via ChIP-seq and immunocytology. Genes with elevated crossover rates and high DMC1 and ASY1 ChIP-seq signals are overrepresented for defense-response and immunity annotations, have higher sequence polymorphism, and exhibit signatures of selection. Our findings are consistent with meiotic recombination promoting genetic diversity, shaping host–pathogen co-evolution, and accelerating adaptation by increasing the efficiency of selection.

FANCM promotes class I interfering crossovers and suppresses class II non-interfering crossovers in wheat meiosis

“…Differential CO rate ( fancm cM/Mb minus wild type cM/Mb), wild type CO rate 43 , and chromatin and meiotic protein mean signals, profiled via ChIP-seq or bisulfite-seq (as analyzed in ref. 33 ), were calculated within each genetic marker interval. Spearman’s rank-order correlation coefficients ( r s ) were computed for each parameter pair and plotted as a correlation matrix, with r s denoted by cell color (R v 4.0.0).…”

“…P v alues for r s correlation coefficients were standardized to represent those based on pairwise values across 100 marker intervals and are indicated within each cell of the correlation matrix. Included data sets are differential CO rate ( fancm cM/Mb minus wild type cM/Mb; “Diff_cMMb”), wild type CO rate derived from a Chinese Spring x Renan genetic map (“IWGSC_cMMb”) 43 , ASY1, DMC1, H3K4me3, H3K9me2 and H3K27me1 ChIP-seq 33 , H3K4me1 and H3K27ac ChIP-seq 60 , H3K27me3 and H3K36me3 ChIP-seq 43 , CENH3 ChIP-seq 61 , whole-genome bisulfite sequencing-derived DNA methylation (mCG, mCHH and mCHG proportions) 43 , and the distance between the midpoint of each marker interval and the midpoint of previously defined centromeric coordinates (“Dist_to_CEN”) 43 . Histone ChIP-seq and bisulfite-seq data are derived from Chinese Spring seedlings or leaf tissue 61 , 43 , 60 , 33 , and ASY1 and DMC1 ChIP-seq data are derived from Chinese Spring immature pre-emergence spikes 33 .…”

“…COs mainly form in gene-rich regions 30 that contain a high frequency of TIR-Mariner transposons 31 and lower levels of DNA polymorphism 32 . COs also correlate with enrichment of the Polycomb histone modification H3K27me3 at the distal ends, indicating a potential role for facultative heterochromatin in shaping the recombination landscape 33 . CO frequency and distribution reduce the probability of creating advantageous novel allelic combinations in crop breeding programmes.…”

Unravelling mechanisms that govern meiotic crossover formation in wheat

“…In wheat, fine-scale mapping of COs revealed an association with a DNA motif specific to the TIR-Mariner transposon family [ 20 ]. In addition, chromatin immunoprecipitation and sequencing (ChIP-seq) of the strand-exchange protein DMC1 (as a proxy for DSB formation) showed significant enrichment close to genes, and an overlap with transposable elements from the Mariner and Mutator families [ 21 ]. However, DMC1 hotspots found in CO-active regions were also strongly enriched for the Polycomb histone mark H3K27me3 [ 21 ].…”

“…In addition, chromatin immunoprecipitation and sequencing (ChIP-seq) of the strand-exchange protein DMC1 (as a proxy for DSB formation) showed significant enrichment close to genes, and an overlap with transposable elements from the Mariner and Mutator families [ 21 ]. However, DMC1 hotspots found in CO-active regions were also strongly enriched for the Polycomb histone mark H3K27me3 [ 21 ]. H3K27me3 is distally enriched on the chromosomes and may play a role in promoting COs in wheat [ 21 ].…”