Crossover Patterning by the Beam-Film Model: Analysis and Implications

Crossing-over is a central feature of meiosis. Meiotic crossover (CO) sites are spatially patterned along chromosomes. CO-designation at one position disfavors subsequent CO-designation(s) nearby, as described by the classical phenomenon of CO interference. If multiple designations occur, COs tend to be evenly spaced. We have previously proposed a mechanical model by which CO patterning could occur. The central feature of a mechanical mechanism is that communication along the chromosomes, as required for CO interference, can occur by redistribution of mechanical stress. Here we further explore the nature of the beam-film model, its ability to quantitatively explain CO patterns in detail in several organisms, and its implications for three important patterning-related phenomena: CO homeostasis, the fact that the level of zero-CO bivalents can be low (the “obligatory CO”), and the occurrence of non-interfering COs. Relationships to other models are discussed.Author Summary: Spatial patterning is a common feature of biological systems at all length scales, from molecular to multi-organismic. Meiosis is the specialized cellular program in which a diploid cell gives rise to haploid gametes for sexual reproduction. Crossing-over between homologous maternal and paternal chromosomes (homologs) is a central feature of this program, playing a role not only for increasing genetic diversity but also for ensuring regular segregation of homologs at the first meiotic division. The distribution of crossovers (COs) along meiotic chromosomes is a paradigmatic example of spatial patterning. Crossovers occur at different positions in different meiotic nuclei but, nonetheless, tend to be evenly spaced along the chromosomes. We previously-described a mechanical “stress and stress relief” model for CO patterning with an accompanying mathematical description (the “beam-film model”). In this paper we explore the roles of mathematical parameters in this model; show that it can very accurately describe experimental data sets from several organisms, in considerably quantitative depth; and discuss implications of the model for several phenomena that are directly related to crossover patterning, including the features which can ensure that every chromosome always acquires at least one crossover.