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

Abstract

<jats:p>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,<jats:italic>asy1/+</jats:italic>heterozygotes also remodel crossovers toward subtelomeric regions at the expense of the pericentromeres. Telomeric recombination increases in<jats:italic>asy1/+</jats:italic>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<jats:italic>asy1/+</jats:italic>, it is undetectable in<jats:italic>asy1</jats:italic>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.</jats:p>

MSH 2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis

“…In order to investigate crossover spacing, we identified cis ‐DCOs from our F 2 genotyping data, by filtering for parental‐heterozygous‐parental genotype transitions (e.g. Col‐Het‐Col or Ler‐Het‐Ler in Col × Ler F 2 individuals; Appendix Fig S1) (Drouaud et al , 2005; Rowan et al , 2019; Lambing et al , 2020a). We generated 2,000 sets of matched randomly generated distances as a control in each case.…”

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

“…6), which suggested that heat induces instability of ASY1-mediated lateral element of SC and ASY4-mediated axis formation through a same signaling pathway. ASY1 loading on chromatin requires the presence and function of ASY3, which in turn relies on ASY4 (Chambon et al, 2018;Ferdous et al, 2012;Lambing et al, 2020a;Yang et al, 2019). It thus is possible that accumulation of ASY3 on chromatin is also interfered, and heat-induced destabilization of ASY1 is a downstream event of the affected ASY4.…”

“…Interactions between ASY1 and ASY4, and ASY4 and ASY3 aid chromatin localizing to the lateral element of SC (Chambon et al, 2018;Yang et al, 2019). Moreover, ASY1 mediates the occurrence of DMC1-dependent MR, and it was recently shown to be essential for maintenance of CO interference (Lambing et al, 2020a;.…”

Comparative Transcriptomic Analysis of Thermally Stressed Arabidopsis thaliana Meiotic Recombination Mutants

“…This suggests that ASY1 and ASY2 may potentially function in tuning the balance between meiotic recombination pathways in response to external cues like heat stress. In Arabidopsis, ASY1 is known to antagonize telomere-led recombination in a dosage-dependent manner [17]. In autotetraploid Arabidopsis arenosa, different ASY1 alleles in uence meiotic chromosome interactions, morphology and axis length [29], and ASY1 is among the key axis component genes that are under strong selection [30].…”

“…3A and 8C) (ASY1 and ASY2 show an increase below the 2-fold cut-off at 28 °C compared to 20 °C in msh4, in contrast to 2.9 and 2.3-fold increases in WT, and 4.6 and 3.5-fold increases in mus81). ASY1 encodes a component of the chromosome axis that forms along the length of replicated sister chromatids during meiosis [15], and is required for proper interhomolog interaction including chromosome pairing, synapsis and recombination [16], as well as ensuring crossover interference [17]. ASY2 is a putative functional homolog of ASY1 [15].…”