Maximizing meiotic crossover rate reveals the map of Crossover Potential

Abstract

Meiotic crossovers are limited in number and unevenly distributed along chromosomes, both features often differing between sexes. The mechanisms imposing a different crossover landscape in female and male meiosis remain elusive. Here, we simultaneously disrupted multiple anti-crossover mechanisms in Arabidopsis and analyzed the whole genome sequence of thousands of female- and male-derived progenies. The largest crossover increase was reached in zyp1 recq4, with 12-fold in females and a 4.5-fold increase in males. Despite this unprecedented level of crossovers, fertility is marginally affected, opening new possibilities for plant breeding. Manipulating additional crossover regulators in zyp1 recq4 did not further elevate the frequency of crossovers, but modified the relative contributions of the two known crossover pathways. This suggests an upper limit was reached and the two pathways compete for a large but limited set of recombination intermediates. Remarkably, while wild-type crossover distribution differs markedly between sexes, the crossover landscapes of diverse mutants in both females and males converge to a single novel profile, which we termed Crossover Potential (COP). The COP profile, which we defined using 49,482 crossovers, can be accurately predicted using only sequence divergence and chromatin features. We propose that the COP represents the density of eligible recombination precursors, which is determined by genomic features and is thus identical in females and males. It suggests that the sexual dimorphism in the crossover landscape results exclusively from differential regulation of the likeness of precursors to mature into crossovers.