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ASY1 acts as a dosage-dependent antagonist of telomere-led recombination and mediates crossover interference in Arabidopsis.

Accepted version
Peer-reviewed

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Article

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Authors

Lambing, Christophe  ORCID logo  https://orcid.org/0000-0001-5218-4217
Kuo, Pallas C 
Topp, Stephanie D 
Henderson, Ian R 

Abstract

During meiosis, interhomolog recombination produces crossovers and noncrossovers 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.

Description

Keywords

ASY1, axis, crossover, interference, meiosis, Arabidopsis, Arabidopsis Proteins, Cell Cycle Proteins, Crossing Over, Genetic, DNA-Binding Proteins, Recombination, Genetic, Telomere

Journal Title

Proc Natl Acad Sci U S A

Conference Name

Journal ISSN

0027-8424
1091-6490

Volume Title

117

Publisher

Proceedings of the National Academy of Sciences

Rights

All rights reserved
Sponsorship
Biotechnology and Biological Sciences Research Council (BB/M004937/1)
European Research Council (681987)
European Research Council (790445)
Biotechnology and Biological Sciences Research Council (BB/S006842/1)
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.