The plant early recombinosome: a high security complex to break DNA during meiosis

The formacion of numerous unpredictable DNA Double Strand Breaks (DSBs) on chromosomes iniciates meiotic recombination. In this perspective, we propose a 'multi-key lock' model to secure the risky but necesary breaks as well as a 'one per pair of cromatids' model for the topoisomerase-like early recombinosome. During meiosis, homologous chromosomes recombine at few sites of crossing-overs (COs) to ensure correct segregation. The initiation of meiotic recombination involves the formation of DNA double strand breaks (DSBs) during prophase I. Too many DSBs are dangerous for genome integrity: if these DSBs are not properly repaired, it could potentially lead to chromosomal fragmentation. Too few DSBs are also problematic: if the obligate CO cannot form between bivalents, catastrophic unequal segregation of univalents lead to the formation of sterile aneuploid spores. Research on the regulation of the formation of these necessary but risky DSBs has recently advanced in yeast, mammals and plants. DNA DSBs are created by the enzymatic activity of the early recombinosome, a topoisomerase-like complex containing SPO11. This opinion paper reviews recent insights on the regulation of the SPO11 cofactors necessary for the introduction of temporally and spatially controlled DSBs. We propose that a 'multi-key-lock' model for each subunit of the early recombinosome complex is required to secure the formation of DSBs. We also discuss the hypothetical implications that the established topoisomerase-like nature of the SPO11 core-complex can have in creating DSB in only one of the two replicated chromatids of early prophase I meiotic chromosomes. This hypothetical 'one per pair of chromatids' DSB formation model could optimize the faithful repair of the self-inflicted DSBs. Each DSB could use three potential intact homologous DNA sequences as repair template: one from the sister chromatid and the two others from the homologous chromosomes.