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

Abstract

Sequence exchange between homologous chromosomes through crossing over and gene conversion is highly conserved among eukaryotes, contributing to genome stability and genetic diversity. Lack of recombination limits breeding efforts in crops, therefore increasing recombination rates can reduce linkage-drag and generate new genetic combinations. We use computational analysis of 13 recombinant inbred mapping populations to assess crossover and gene conversion frequency in the hexaploid genome of wheat (Triticum aestivum). We observe that high frequency crossover sites are shared between populations and that closely related parental founders lead to populations with more similar crossover patterns. We demonstrate that gene conversion is more prevalent and covers more of the genome in wheat than in other plants, making it a critical process in the generation of new haplotypes, particularly in centromeric regions where crossovers are rare. We have identified QTL for altered gene conversion and crossover frequency and confirm functionality for a novel RecQ helicase gene that belongs to an ancient clade that is missing in some plant lineages including Arabidopsis. This is the first gene to be demonstrated to be involved in gene conversion in wheat. Harnessing the RecQ helicase has the potential to break linkage-drag utilizing widespread gene conversions. Main Text:There is an evolutionary requirement for genetic diversity across a species. Shuffling of material between homologous chromosomes, or genetic recombination, breaks linkage between genes resulting in offspring that have combinations of alleles that differ from those found in either of the parents. During meiosis, double-strand breaks (DSBs) can generate sequence variation in gametes via the DSB repair model (Szostak et al., 1983). DSBs are resolved either by homologous recombination as crossovers (COs) i.e. the reciprocal exchange of large regions between chromosomes, or otherwise as non-crossovers (NCOs). A minimum of one CO per chromosome during meiosis is a requirement for proper chromosome segregation (Pardo-Manuel De Villena and Sapienza, 2001). When both COs and NCOs are resolved, they can also give rise to gene conversions (GCs) as a mechanism of DSB repair involving the non-reciprocal transfer of short DNA segments between homologous non-sister chromatids (Sun et al., 2012;Halldorsson et al., 2016). GCs can be

Natural variation in meiotic recombination rate shapes introgression patterns in intraspecific hybrids between wild and domesticated barley

“…S4). This is in strong agreement with previous studies reporting positive correlations between SNP density, recombination frequency and gene density in other small‐ or large‐genome plants (Mascher et al ., 2017; Darrier et al ., 2017; Jordan et al ., 2018; Kianian et al ., 2018; Gardiner et al ., 2019; Rowan et al ., 2019). Given the suppressive effects of chromosomal inversions, their rather low frequency and small size (few Mb) previously shown in barley make them unlikely to contribute to genome‐wide differences in recombination patterning (Konishi & Linde‐Laursen, 1988; Keilwagen et al ., 2019).…”

“…Using this approach, we were associating the number of crossovers accumulated over nine meiotic divisions with the genotypic constitution of the final generation (BC 1 S 3:8 ), which did not allow us to determine whether a recombination rate modifier was present/absent or homozygous/heterozygous throughout previous meiotic divisions. Therefore, as already argued by others, we are systematically underestimating the effects of recombination rate modifiers and are only detecting dominant modifiers with strong effects (Esch et al ., 2007; Jordan et al ., 2018; Gardiner et al ., 2019). Furthermore, to identify trans ‐acting recombination rate modifiers rather than identifying common recombination breakpoints, we applied a cross‐validation step in which SNPs of a given chromosome were only screened for associations with the number of crossovers on the remaining six chromosomes (Jordan et al ., 2018).…”

Evolution of recombination landscapes in diverging populations of bread wheat

“…Our results are consistent with previous reports. Gardiner et al (2019) showed that closely-related bread wheat parental lines lead to RIL populations with more similar crossover profiles. (Darrier et al (2017) compared LD-based recombination profiles of a European and an Asian population, the two main ancestral bread wheat genetic pools, on two scaffolds of 1.2 and 2.5 Mb on chromosome 3B.…”

Bread wheat TaSPO11‐1 exhibits evolutionarily conserved function in meiotic recombination across distant plant species

“…Until now, only a dozen of genes ( TaRAD51 , TaRAD51C , TaRAD51D , TaDMC1 , TaMRE11 , TaRAD50 , TaASY1 , TaZYP1 , TaPHS1 , TaPh1 , TaREC8 and TaRECQ‐7 ), among more than 100 known as involved in meiotic recombination in plants, have been cloned and significantly analysed in wheat. These analyses have mainly been limited to comparisons of sequences of homoeologous copies, expression analyses and immunolocalization (Boden et al ., 2007; de Bustos et al ., 2007; Boden et al ., 2009; Devisetty et al ., 2010; Perez et al ., 2011; Khoo et al ., 2012a; Khoo et al ., 2012b; Ma et al ., 2018; Gardiner et al ., 2019). TaPh1 , which controls homoeologous recombination in wheat, remains the best‐defined locus involved in meiosis in wheat (Griffiths et al ., 2006; Moore, 2014; Martin et al ., 2017).…”