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
.
Crossovers (COs) ensure accurate chromosome segregation during meiosis while creating novel allelic combinations. Here, we show that allotetraploid (AABB) durum wheat (Triticum turgidum ssp. durum) utilizes two pathways of meiotic recombination. The class I pathway requires MSH4 and MSH5 (MutSg) to maintain the obligate CO/chiasma and accounts for ;85% of meiotic COs, whereas the residual ;15% are consistent with the class II CO pathway. Class I and class II chiasmata are skewed toward the chromosome ends, but class II chiasmata are significantly more distal than class I chiasmata. Chiasma distribution does not reflect the abundance of double-strand breaks, detected by proxy as RAD51 foci at leptotene, but only ;2.3% of these sites mature into chiasmata. MutSg maintains the obligate chiasma despite a 5.4-kb deletion in MSH5B rendering it nonfunctional, which occurred early in the evolution of tetraploid wheat and was then domesticated into hexaploid (AABBDD) common wheat (Triticum aestivum), as well as an 8-kb deletion in MSH4D in hexaploid wheat, predicted to create a nonfunctional pseudogene. Stepwise loss of MSH5B and MSH4D following hybridization and whole-genome duplication may have occurred due to gene redundancy (as functional copies of MSH5A, MSH4A, and MSH4B are still present in the tetraploid and MSH5A, MSH5D, MSH4A, and MSH4B are present in the hexaploid) or as an adaptation to modulate recombination in allopolyploid wheat.
FANCM suppresses crossovers in plants by unwinding recombination intermediates. In wheat, crossovers are skewed toward the chromosome ends, thus limiting generation of novel allelic combinations. Here, we observe that FANCM maintains the obligate crossover in tetraploid and hexaploid wheat, thus ensuring that every chromosome pair exhibits at least one crossover, by localizing class I crossover protein HEI10 at pachytene. FANCM also suppresses class II crossovers that increased 2.6-fold in fancm msh5 quadruple mutants. These data are consistent with a role for FANCM in second-end capture of class I designated crossover sites, whilst FANCM is also required to promote formation of non-crossovers. In hexaploid wheat, genetic mapping reveals that crossovers increase by 31% in fancm compared to wild type, indicating that fancm could be an effective tool to accelerate breeding. Crossover rate differences in fancm correlate with wild type crossover distributions, suggesting that chromatin may influence the recombination landscape in similar ways in both wild type and fancm.
The output can be accessed at: https://repository.rothamsted.ac.uk/item/96x11/acytological-analysis-of-wheat-meiosis-targeted-by-virus-induced-gene-silencing-vigs.
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