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

Abstract

During meiosis, crossovers (COs) create new allele associations by reciprocal exchange of DNA. In bread wheat (Triticum aestivum L.), COs are mostly limited to subtelomeric regions of chromosomes, resulting in a substantial loss of breeding efficiency in the proximal regions, though these regions carry 60-70% of the genes. Identifying sequence and/or chromosome features affecting recombination occurrence is thus relevant to improve and drive recombination. Using the recent release of a reference sequence of chromosome 3B and of the draft assemblies of the 20 other wheat chromosomes, we performed fine-scale mapping of COs and revealed that 82% of COs located in the distal ends of chromosome 3B representing 19% of the chromosome length. We used 774 SNPs to genotype 180 varieties representative of the Asian and European genetic pools and a segregating population of 1270 F 6 lines. We observed a common location for ancestral COs (predicted through linkage disequilibrium) and the COs derived from the segregating population. We delineated 73 small intervals (,26 kb) on chromosome 3B that contained 252 COs. We observed a significant association of COs with genic features (73 and 54% in recombinant and nonrecombinant intervals, respectively) and with those expressed during meiosis (67% in recombinant intervals and 48% in nonrecombinant intervals). Moreover, while the recombinant intervals contained similar amounts of retrotransposons and DNA transposons (42 and 53%), nonrecombinant intervals had a higher level of retrotransposons (63%) and lower levels of DNA transposons (28%). Consistent with this, we observed a higher frequency of a DNA motif specific to the TIR-Mariner DNA transposon in recombinant intervals. KEYWORDS recombination; meiosis; bread wheat; linkage disequilibrium; transposon; hotspot; sequence motif M EIOTIC recombination is a process that allows reshuffling of diversity by the reciprocal exchange of DNA called a crossover (CO). This phenomenon is conserved in most eukaryotes (for a review see Mercier et al. 2015) and follows the formation of a double-strand break (DSB) of DNA generated by the topoisomerase SPO11 complex. However, the number of DSBs is at least 10-to 50-fold greater than the number of COs which rarely exceeds three per bivalent chromosome per meiosis (Mercier et al. 2015). This paucity of COs per meiosis with regards to the number of DSBs suggests the existence of a tight control and regulation of recombination in plants that promote DSB repair in a manner that does not lead to COs. For example, the study of the two helicases AtFANCM and RECQ4 (AtRECQ4A and AtRECQ4B) (Crismani et al. 2012;Knoll et al. 2012;Girard et al. 2014;Séguéla-Arnaud et al. 2015) revealed three-and sixfold CO frequency increases in the Atfancm single mutant and the Atrecq4a/Atrecq4b double mutant, respectively, compared to the wild type. These increases result from additional COs from the class-II pathway which suggests that FANCM and RECQ4 prevent CO formation and direct recombination intermediates towar...

Analysis of the recombination landscape of hexaploid bread wheat reveals genes controlling recombination and gene conversion frequency

“…Using the 35K array we see the characteristic normal distribution of CO frequency, with an average of 41-52 COs per RIL, and a non-random distribution of COs between RILs and along the chromosomes (Huang et al, 2012;Esch et al, 2007;Darrier et al, 2017). There is a positive correlation between the number of genes in the CO interval and the number of RILs with the CO suggesting that perhaps recombination in gene rich regions leads to favourable phenotypes that are under selective pressure.…”

“…It is therefore important for us to understand recombination and GC if we are to alter their rates to accelerate the induction of novel allelic combinations or to generate stable cultivars. This is particularly important in bread wheat where recombination frequency is low and skewed toward the ends of chromosomes (Darrier et al, 2017). Wheat has a large (16Gb) complex allohexaploid genome and, in the light of recent advances in the wheat's genomic and genetic resources, it presents an excellent model crop (Brenchley et al, 2012;Clavijo et al, 2017;Krasileva et al, 2017;IWGSC et al 2018.…”

Impact of transposable elements on genome structure and evolution in bread wheat

“…At this point, we can only speculate about the possible impact of meiotic recombination as a driving force towards maintaining a stable chromosome organization. Previous studies have shown that recombination in highly repetitive genomes occurs mainly in or near genes [39]. Thus, it might be important that spacing of genes is preserved for proper expression regulation or proper pairing during meiosis.…”

A wheat dominant dwarfing line with Rht12, which reduces stem cell length and affects gibberellic acid synthesis, is a 5AL terminal deletion line

“…Rht‐B1c ( Rht3 ), Rht‐D1c ( Rht10 ), Rht‐B1e ( Rht11 ) and Rht‐B1p ( Rht17 ) are orthologs of Rht‐B1b or Rht‐D1b (Bazhenov et al ., ; Wu et al ., ; Divashuk et al ., ; Li et al ., ,b, ). Fine mapping and map‐based cloning in wheat have become easier following the release of the Chinese Spring (CS, a wheat variety) genomic sequences by IWGSC (Darrier et al ., ), but to date no Rht gene has been isolated by map‐based cloning.…”