Distal Bias of Meiotic Crossovers in Hexaploid Bread Wheat Reflects Spatio-Temporal Asymmetry of the Meiotic Program

Abstract

Meiotic recombination generates genetic variation and provides physical links between homologous chromosomes (crossovers) essential for accurate segregation. In cereals the distribution of crossovers, cytologically evident as chiasmata, is biased toward the distal regions of chromosomes. This creates a bottleneck for plant breeders in the development of varieties with improved agronomic traits, as genes situated in the interstitial and centromere proximal regions of chromosomes rarely recombine. Recent advances in wheat genomics and genome engineering combined with well-developed wheat cytogenetics offer new opportunities to manipulate recombination and unlock genetic variation. As a basis for these investigations we have carried out a detailed analysis of meiotic progression in hexaploid wheat (Triticum aestivum) using immunolocalization of chromosome axis, synaptonemal complex and recombination proteins. 5-Bromo-2′-deoxyuridine (BrdU) labeling was used to determine the chronology of key events in relation to DNA replication. Axis morphogenesis, synapsis and recombination initiation were found to be spatio-temporally coordinated, beginning in the gene-dense distal chromosomal regions and later occurring in the interstitial/proximal regions. Moreover, meiotic progression in the distal regions was coordinated with the conserved chromatin cycles that are a feature of meiosis. This mirroring of the chiasma bias was also evident in the distribution of the gene-associated histone marks, H3K4me3 and H3K27me3; the repeat-associated mark, H3K27me1; and H3K9me3. We believe that this study provides a cytogenetic framework for functional studies and ongoing initiatives to manipulate recombination in the wheat genome.

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

“…Distal ChIP-seq enrichment is consistent with immunolocalization of DMC1 and ASY1, showing telomere-biased accumulation early in prophase I ( Fig. 2 A,B; Osman et al 2021 ). DMC1 and ASY1 chromosome-scale profiles positively correlate with crossover rate (cM/Mb) derived from a Chinese Spring × Renan F 6 genetic map (genome-wide r s = 0.80 and 0.75, respectively) ( IWGSC 2018 ), as well as with gene density and markers of euchromatin (H3K4me1, H3K4me3, and H3K27ac) and facultative heterochromatin (H3K27me3) ( Fig.…”

The E3 ubiquitin ligase DESYNAPSIS1 regulates synapsis and recombination in rice meiosis

“…In rice, SC-like polycomplexes were temporarily observed in late-leptotene meiocytes of the wild-type, and can also be continuously detected in the dsnp1 mutant. In other plants, a similar loading pattern of the TF proteins during leptotene/zygotene transition is reported in Brassica oleracea and Triticum aestivum (Lambing et al, 2015;Osman et al, 2021), further implying that precocious assembly of SC proteins may be a universal phenomenon.…”

Rewiring Meiosis for Crop Improvement

“…The CO landscape in cereals is distinct from Arabidopsis and COs are exclusively formed in distal ends of the chromosomes ( Figure 1 ; Phillips et al, 2015 ; Osman et al, 2021 ). Moreover, the spatio-temporal formation of the chromosome axis which is observed from immunostaining of ASY1, the deposition of ZYP1 which marks synapsis between homologous chromosomes, and the formation of DSBs differ significantly between cereals and Arabidopsis ( Figures 1A , C ).…”

“…Moreover, the spatio-temporal formation of the chromosome axis which is observed from immunostaining of ASY1, the deposition of ZYP1 which marks synapsis between homologous chromosomes, and the formation of DSBs differ significantly between cereals and Arabidopsis ( Figures 1A , C ). For example, axis, synapsis, and DSB formation are initiated on the distal regions before being detected on the interstitial and centromere-proximal regions in barley and wheat ( Higgins et al, 2012 ; Lambing et al, 2017 ; Desjardins et al, 2020 ; Osman et al, 2021 ). In contrast, no polarization of axis formation or DSB formation is detected in Arabidopsis ( Lambing et al, 2017 ; Figure 1A ).…”

“…If conserved in plants, this propensity of SPO11 may further reduce the targeted effect. Moreover, barley and wheat chromosome axes initiate first in distal regions in early prophase ( Higgins et al, 2012 ; Osman et al, 2021 ). It is unknown whether SPO11 is functionally active to form a DSB without a chromosome axis when recruited in centromere-proximal regions at an early stage of meiosis.…”