Sex-Specific Crossover Distributions and Variations in Interference Level along Arabidopsis thaliana Chromosome 4

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Abstract
In many species, sex-related differences in crossover (CO) rates have been described at chromosomal and regional levels. In this study, we determined the CO distribution along the entire Arabidopsis thaliana Chromosome 4 (18 Mb) in male and female meiosis, using high density genetic maps built on large backcross populations (44 markers, >1,300 plants). We observed dramatic differences between male and female map lengths that were calculated as 88 cM and 52 cM, respectively. This difference is remarkably parallel to that between the total synaptonemal complex lengths measured in male and female meiocytes by immunolabeling of ZYP1 (a component of the synaptonemal complex). Moreover, CO landscapes were clearly different: in particular, at both ends of the map, male CO rates were higher (up to 4-fold the mean value), whereas female CO rates were equal or even below the chromosomal average. This unique material gave us the opportunity to perform a detailed analysis of CO interference on Chromosome 4 in male and female meiosis. The number of COs per chromosome and the distances between them clearly departs from randomness. Strikingly, the interference level (measured by coincidence) varied significantly along the chromosome in male meiosis and was correlated to the physical distance between COs. The significance of this finding on the relevance of current CO interference models is discussed. Meiotic crossovers between homologous chromosomes ensure their proper segregation to generate ultimately gametes. They also create new allelic combinations which contribute to the diversity of traits among individuals. In all eukaryotes, the number and the localization of crossovers along chromosomes are not random. In addition, crossovers are not independent of each other: the occurrence of a crossover lowers the probability that another crossover arises in its vicinity. The mechanism of this phenomenon, called “crossover interference,” is one of the most challenging puzzles that geneticists have been faced with in the last century. In this paper, we precisely described the distribution of crossovers along Chromosome 4 of the model plant species Arabidopsis thaliana, separately in male and female meiosis. Interestingly, we observed that crossovers are 1.7 more numerous in male than in female meiosis, and this increase is especially marked at the ends of the chromosome. Moreover, our results provide the first evidence that the level of interference along a chromosome is not a constant and is correlated with the physical distance between crossovers. These results shed new light on the determinism of crossover localization and could have important outcomes on the relevance of current models of crossover interference.