MSH 2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis

Abstract

During meiosis, DNA double‐strand breaks undergo interhomolog repair to yield crossovers between homologous chromosomes. To investigate how interhomolog sequence polymorphism affects crossovers, we sequenced multiple recombinant populations of the model plant Arabidopsis thaliana . Crossovers were elevated in the diverse pericentromeric regions, showing a local preference for polymorphic regions. We provide evidence that crossover association with elevated diversity is mediated via the Class I crossover formation pathway, although very high levels of diversity suppress crossovers. Interhomolog polymorphism causes mismatches in recombining molecules, which can be detected by MutS homolog (MSH) mismatch repair protein heterodimers. Therefore, we mapped crossovers in a msh2 mutant, defective in mismatch recognition, using multiple hybrid backgrounds. Although total crossover numbers were unchanged in msh2 mutants, recombination was remodelled from the diverse pericentromeres towards the less‐polymorphic sub‐telomeric regions. Juxtaposition of megabase heterozygous and homozygous regions causes crossover remodelling towards the heterozygous regions in wild type Arabidopsis , but not in msh2 mutants. Immunostaining showed that MSH 2 protein accumulates on meiotic chromosomes during prophase I, consistent with MSH2 regulating meiotic recombination. Our results reveal a pro‐crossover role for MSH 2 in regions of higher sequence diversity in A. thaliana .

FISH landmarks reflecting meiotic recombination and structural alterations of chromosomes in wheat (Triticum aestivum L.)

“…Even in the mutants of anticrossover genes, recombination was prevented in regions with the highest sequence divergence, displayed by SNP [ 3 ]. In Arabidopsis , the msh2 (MutS-related heterodimers) mutant displayed significantly reduced SNP enrichment around crossovers compared with the wild type [ 26 ]. These studies indicated that SNP polymorphisms and indels are important factors affecting meiotic recombination.…”

Preferential meiotic chromosome pairing among homologous chromosomes with cryptic sequence variation in tetraploid maize

“…However, the sequence‐polymorphism‐mediated suppression of crossovers is dependent on the chromosome location and local chromatin environment (Serra et al ., 2018). A recent study using multiple recombination populations in Arabidopsis thaliana revealed that crossovers were elevated in the diverse pericentromeric regions (Blackwell et al ., 2020). In addition, recombination was remodeled from the pericentromeric regions towards the less‐polymorphic sub‐telomeric regions in the mutation background of MSH2 , a key DNA mismatch repair gene (Blackwell et al ., 2020).…”

“…A recent study using multiple recombination populations in Arabidopsis thaliana revealed that crossovers were elevated in the diverse pericentromeric regions (Blackwell et al ., 2020). In addition, recombination was remodeled from the pericentromeric regions towards the less‐polymorphic sub‐telomeric regions in the mutation background of MSH2 , a key DNA mismatch repair gene (Blackwell et al ., 2020). These results suggest that the location of sequence polymorphism along the chromosomes may also impact level of preferential pairing among different homologous chromosomes.…”

Rewiring Meiosis for Crop Improvement

“…This strategy was successfully transferred into crops with recq4 mutant showing a significant increase in crossover frequency in rice, tomato, and pea ( Mieulet et al, 2018 ; De Maagd et al, 2020 ). Surprisingly, the extra COs formed in anti-class II CO mutants are present in regions with low degree of polymorphism ( Fernandes et al, 2018 ; Blackwell et al, 2020 ). In particular, fancm recombination phenotype seems to be sensitive to the hybrid context as it can be detected in brassica, pea, and rice but not in Arabidopsis, tomato and wheat hybrid lines.…”