MutS homologue 4 and MutS homologue 5 Maintain the Obligate Crossover in Wheat Despite Stepwise Gene Loss following Polyploidization

Crossovers (COs) ensure accurate chromosome segregation during meiosis while creating novel allelic combinations. Here, we show that allotetraploid (AABB) durum wheat ( ssp. ) utilizes two pathways of meiotic recombination. The class I pathway requires MSH4 and MSH5 (MutSγ) 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. MutSγ maintains the obligate chiasma despite a 5.4-kb deletion in rendering it nonfunctional, which occurred early in the evolution of tetraploid wheat and was then domesticated into hexaploid (AABBDD) common wheat ( ), as well as an 8-kb deletion in in hexaploid wheat, predicted to create a nonfunctional pseudogene. Stepwise loss of and following hybridization and whole-genome duplication may have occurred due to gene redundancy (as functional copies of , , and are still present in the tetraploid and , , , and are present in the hexaploid) or as an adaptation to modulate recombination in allopolyploid wheat.