MUS81 is required for atypical recombination intermediate resolution but not crossover designation in rice

Abstract

Summary The endonuclease methyl methanesulfonate and UV‐sensitive protein 81 (MUS81) has been reported to participate in DNA repair during mitosis and meiosis. However, the exact meiotic function of MUS81 in rice remains unclear. Here, we use a combination of physiological, cytological, and genetic approaches to provide evidence that MUS81 functions in atypical recombination intermediate resolution rather than crossover designation in rice. Cytological and genetic analysis revealed that the total chiasma numbers in mus81 mutants were indistinguishable from wild‐type. The numbers of HEI10 foci (the sites of interference‐sensitive crossovers) in mus81 were also similar to that of wild‐type. Moreover, disruption of MUS81 in msh5 or msh4 msh5 background did not further decrease chiasmata frequency, suggesting that rice MUS81 did not function in crossover designation. Mutation of FANCM and ZEP1 could enhance recombination frequency. Unexpectedly, chromosome fragments and bridges were frequently observed in mus81 zep1 and mus81 fancm, illustrating that MUS81 may resolve atypical recombination intermediates. Taken together, our data suggest that MUS81 contributes little to crossover designation but plays a crucial role in the resolution of atypical meiotic intermediates by working together with other anti‐crossover factors.

Crossover interference mechanism: New lessons from plants

“…In rice, GEN1, the homolog of the Holliday junction resolvase is necessary for class II CO formation (Wang et al, 2017) while it is not in Arabidopsis (Bauknecht and Kobbe, 2014;Olivier et al, 2016), suggesting that the MUS81 pathways have diverged between dicots and monocots. Compared to Arabidopsis, the MUS81 pathway contributes even less to CO designation in rice (Wang et al, 2017;Mu et al, 2022), suggesting that the weight of the different pathways described in this review probably depend on each species.…”

“…It has been proposed that these dissolution pathways leading to NCO could be especially important for multi-invasion complexes formed between more than two DNA molecules that would otherwise lead to aberrant recombination intermediates (Emmenecker et al, 2022;Mu et al, 2022). Whether or not these pathways could be involved in a putative chromatid interference phenomenon (Zhao et al, 1995;Sarens et al, 2021) is still unknown.…”

FIGL1 attenuates meiotic interhomolog repair and is counteracted by RAD51 paralog XRCC2 and chromosome axis protein ASY1 during meiosis

“…FIGL1 is, however, essential for meiotic DSB repair in different crop plants, including rice figl1 mutant showing chromosome fragmentation at metaphase I (64, 66). These unrepaired breaks might result from complex DMC1-and RAD51-mediated interhomolog invasions, which MUS81 is unable to repair, given a more considerable genome complexity and chromosome number in rice (74). Our data provide evidence that the RAD51-dependent pathway promotes accurate meiotic repair outcomes in Arabidopsis figl1 .…”

FANCM interacts with the MHF1‐MHF2 complex to limit crossover frequency during rice meiosis

“…It was reported that rice msh4 has the least residual chiasmata frequent among zmm mutants and the distribution of residual chiasmata is consistent with a Poissonpredicted distribution (Mu et al, 2023;Zhang et al, 2014). To further confirm rice fancm limits class II crossovers, we counted the distribution of chiasmata present in the fancm msh4 double mutant using previously described criteria (Sanchez Moran et al, 2001).…”