HEI10 coarsening, chromatin and sequence polymorphism shape the plant meiotic recombination landscape

Morgan, Chris; Howard, Martin; Henderson, Ian R.

doi:10.1016/j.pbi.2024.102570

Cited by 4 publications

References 72 publications

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

Rafiei,

Ronceret

2024

Plant Reprod

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Key message 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. Abstract 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.

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

Rafiei,

Ronceret

2024

Plant Reprod

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Meiosis in plants: From understanding to manipulation

Chen,

Wang,

Wang

2025

New Crops

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Genetic dissection of MutL complexes in Arabidopsis meiosis

Kbiri,

Fernández-Jiménez,

Dziegielewski

et al. 2024

Preprint

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During meiosis, homologous chromosomes exchange genetic material through crossing-over. The main crossover pathway relies on ZMM proteins, including ZIP4 and HEI10, and is typically resolved by the MLH1/MLH3 heterodimer, MutLγ. Our analysis of plant fertility and bivalent formation revealed that the MUS81 endonuclease can partially compensate for the MutLγ loss. Comparing genome-wide crossover maps of the mlh1 mutant with ZMM-deficient mutants and lines with varying HEI10 levels reveals that while crossover interference persists in mlh1, it is weakened. Additionally, mlh1 show reduced crossover assurance, leading to a higher incidence of aneuploidy in offspring. This is likely due to MUS81 resolving intermediates without the crossover bias seen in MutLγ. Comparing mlh1 mlh3 mus81 and zip4 mus81 mutants suggests that additional crossover pathways emerge in the absence of both MutLγ and MUS81. The loss of MutLγ can also be suppressed by eliminating the FANCM helicase. Elevated expression of MLH1 or MLH3 increases crossover frequency, while their overexpression significantly reduces crossover numbers and plant fertility, highlighting the importance for tight control of MLH1/MLH3 levels. By contrast, PMS1, a component of the MutLα endonuclease, appears not to be involved in crossing-over. Together, these findings demonstrate the unique role of MutLγ in ZMM-dependent crossover regulation.

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HEI10 coarsening, chromatin and sequence polymorphism shape the plant meiotic recombination landscape

Cited by 4 publications

References 72 publications

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

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

Meiosis in plants: From understanding to manipulation

Genetic dissection of MutL complexes in Arabidopsis meiosis

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