ASY1 acts as a dosage-dependent antagonist of telomere-led recombination and mediates crossover interference in Arabidopsis.
Proceedings of the National Academy of Sciences of the United States of America
National Academy of Sciences
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Lambing, C., Kuo, P. C., Tock, A., Topp, S. D., & Henderson, I. (2020). ASY1 acts as a dosage-dependent antagonist of telomere-led recombination and mediates crossover interference in Arabidopsis.. Proceedings of the National Academy of Sciences of the United States of America, 117 (24), 13647-13658. https://doi.org/10.1073/pnas.1921055117
During meiosis, interhomolog recombination produces crossovers and noncross-overs to create genetic diversity. Meiotic recombination frequency varies at multiple scales, with high subtelomeric recombination and suppressed centromeric recombination typical in many eukaryotes. During recombination, sister chromatids are tethered as loops to a polymerized chromosome axis, which, in plants, includes the ASY1 HORMA domain protein and REC8-cohesin complexes. Using chromatin immunoprecipitation, we show an ascending telomere-to-centromere gradient of ASY1 enrichment, which correlates strongly with REC8-cohesin ChIP-seq data. We mapped crossovers genome-wide in the absence of ASY1 and observe that telomere-led recombination becomes dominant. Surprisingly, asy1/+ heterozygotes also remodel crossovers toward subtelomeric regions at the expense of the pericentromeres. Telomeric recombination increases in asy1/+ occur in distal regions where ASY1 and REC8 ChIP enrichment are lowest in wild type. In wild type, the majority of crossovers show interference, meaning that they are more widely spaced along the chromosomes than expected by chance. To measure interference, we analyzed double crossover distances, MLH1 foci, and fluorescent pollen tetrads. Interestingly, while crossover interference is normal in asy1/+, it is undetectable in asy1 mutants, indicating that ASY1 is required to mediate crossover interference. Together, this is consistent with ASY1 antagonizing telomere-led recombination and promoting spaced crossover formation along the chromosomes via interference. These findings provide insight into the role of the meiotic axis in patterning recombination frequency within plant genomes.
Telomere, Arabidopsis, Cell Cycle Proteins, DNA-Binding Proteins, Arabidopsis Proteins, Recombination, Genetic, Crossing Over, Genetic
Research was supported by grants from the European Research Council Consolidator award SynthHotSpot and Proof-of-Concept award HEIREC and BBSRC ERA-CAPs Grant BB/M004937/1.
ECH2020 EUROPEAN RESEARCH COUNCIL (ERC) (681987)
European Commission Horizon 2020 (H2020) ERC (790445)
External DOI: https://doi.org/10.1073/pnas.1921055117
This record's URL: https://www.repository.cam.ac.uk/handle/1810/305803
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