Meiotic chromosome organization and crossover patterns

Abstract

Meiosis is the foundation of sexual reproduction, and crossover recombination is one hallmark of meiosis. Crossovers establish the physical connections between homolog chromosomes (homologs) for their proper segregation and exchange DNA between homologs to promote genetic diversity in gametes and thus progenies. Aberrant crossover patterns, e.g. absence of the obligatory crossover, are the leading cause of infertility, miscarriage, and congenital disease. Therefore, crossover patterns have to be tightly controlled. During meiosis, loop/axis organized chromosomes provide the structural basis and regulatory machinery for crossover patterning. Accumulating evidence shows that chromosome axis length regulates not only the numbers but also the positions of crossovers. In addition, recent studies suggest that alterations in axis length and the resultant alterations in crossover frequency may contribute to evolutionary adaptation. Here, current advances regarding these issues are reviewed, the possible mechanisms for axis length regulating crossover frequency are discussed, and important issues that need further investigations are suggested.

Per-nucleus crossover covariation is regulated by chromosome organization

“…A chromosome usually obtains at least one CO, the obligatory CO, regardless of its axis length ( Jones and Franklin, 2006 ; Zhang et al., 2014a ). The maximal number of COs on a chromosome is largely determined by the interplay between the axis length and CO interference distance ( Wang et al., 2021a ; Shang et al., 2022 ). When the axis length is less than the interference distance, that is, interference can spread outward to both ends of the chromosome, this chromosome can get only one CO.…”

“…A general positive correlation between chromosome axis length and CO frequency leads to the hypothesis that variations in axis length are a major contributor to CO variation ( Kleckner et al., 2003 ). Accumulated evidence supports this general idea: alterations in chromosomes axis length always result in coordinate alterations in CO frequency; however, alterations in DSBs and/or DSB-mediated recombination intermediates do not change axis length and CO formation only have subtle effects on local chromosome axis length (reviewed in Wang et al., 2021a ; Shang et al., 2022 ). Consistently, human female meiosis has a longer chromosome axis and consequently more COs than male meiosis ( Figure S1 B) (e.g., Bojko, 1985 ; Lynn et al., 2004 ; Tease and Hultén, 2004 ; Codina-Pascual et al., 2006 ; Gruhn et al., 2013 ; Wang et al., 2017 , 2019c ).…”

“…Recently, we have shown that gradual alterations in axis lengths result in coordinate and gradual alterations in the numbers of meiotic DSBs and COs ( Song et al., 2021 ; Wang et al., 2021b ). The axis length also regulates CO distributions along chromosomes, for example, COs tend to be more distally located on short chromosomes ( Wang et al., 2021a ; Shang et al., 2022 ). However, how chromosome axis length is regulated is unclear.…”

Dual control of meiotic crossover patterning

“…Interestingly in some species, such as humans or Arabidopsis, CO number differs in males and females. This heterochiasmy correlates with axis/SC length, with the number of COs proportional to axis length 4,16,17 . CO interference appears to propagate at a similar axis/SC distance (µm) in both sexes, which means that interference acts over greater genomic ranges (DNA) in the sex with a shorter axis/SC 17,18 , an observation which shows that the relevant space for the mechanism of interference is the axis/SC length.…”

“…SC length has been shown to correlate with the frequency of class I COs 4,16,17 . We wondered if the class I CO increase provoked by zyp1 and HEI10 oe is associated with variation in SC length.…”