ASY1 acts as a dosage-dependent antagonist of telomere-led recombination and mediates crossover interference in Arabidopsis.
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Publication Date
2020-06-04Journal Title
Proceedings of the National Academy of Sciences of the United States of America
ISSN
0027-8424
Publisher
National Academy of Sciences
Volume
117
Issue
24
Pages
13647-13658
Language
eng
Type
Article
This Version
AM
Physical Medium
Print-Electronic
Metadata
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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
Abstract
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.
Keywords
Telomere, Arabidopsis, Cell Cycle Proteins, DNA-Binding Proteins, Arabidopsis Proteins, Recombination, Genetic, Crossing Over, Genetic
Sponsorship
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.
Funder references
BBSRC (BB/M004937/1)
ECH2020 EUROPEAN RESEARCH COUNCIL (ERC) (681987)
European Commission Horizon 2020 (H2020) ERC (790445)
Identifiers
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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