The Role of Chromatid Interference in Determining Meiotic Crossover Patterns

Abstract

Plants, like all sexually reproducing organisms, create genetic variability by reshuffling parental alleles during meiosis. Patterns of genetic variation in the resulting gametes are determined by the independent assortment of chromosomes in meiosis I and by the number and positioning of crossover (CO) events during meiotic recombination. On the chromosome level, spatial distribution of CO events is biased by multiple regulatory mechanisms, such as CO assurance, interference and homeostasis. However, little is known about how multiple COs are distributed among the four chromatids of a bivalent. Chromatid interference (CI) has been proposed as a regulatory mechanism that biases distribution of multiple COs toward specific chromatid partners, however, its existence has not been well-studied and its putative mechanistic basis remains undescribed. Here, we introduce a novel method to quantitatively express CI, and take advantage of available tetrad-based genotyping data from Arabidopsis and maize male meiosis to quantify CI effects on a genome-wide and chromosomal scale. Overall, our analyses reveal random involvement of sister chromatids in double CO events across paired chromosomes, indicating an absence of CI. However, on a genome-wide level, CI was found to vary with physical distance between COs, albeit with different effects in Arabidopsis and maize. While effects of CI are minor in Arabidopsis and maize, the novel methodology introduced here enables quantitative interpretation of CI both on a local and genome-wide scale, and thus provides a key tool to study CI with relevance for both plant genetics and crop breeding.

Remarkably high rate of meiotic recombination in the fission yeastSchizosaccharomyces pombe

“…As described above, when considering two adjacent COs, three types of outcomes would be expected depending on how many chromatids are affected (2C-DCOs, 3C-DCOs and 4C-DCOs, Figure S6). In the absence of chromatid interference, DCOs are randomly distributed among the four chromatids of the bivalent, and the three types of DCOs will give a ratio of 1:2:1 (2C:3C:4C DCOs) [33]. If the chromatid implicated in a CO affects somehow the choice of the chromatid of the adjacent CO, we would expect a deviation from this ratio.…”

Cosegregation of recombinant chromatids maintains genome-wide heterozygosity in an asexual nematode

“…Consequently, co-orientation of recombinant chromatids could also be at play in monocentric species. However, in species that establish multiple crossovers between all chromatids within a pair of homologs ( 35 ), which is restricted to monocentric species, there will be no possibility to cosegregate the recombinants together. Hence, CRC can probably emerge only in species that initially have a limited number of crossovers per chromosome, as previously proposed ( 6 ), or at least multiple crossovers restricted to a single pair of chromatids.…”

Crossover interference mechanism: New lessons from plants

“…It has been proposed that these dissolution pathways leading to NCO could be especially important for multi-invasion complexes formed between more than two DNA molecules that would otherwise lead to aberrant recombination intermediates (Emmenecker et al, 2022;Mu et al, 2022). Whether or not these pathways could be involved in a putative chromatid interference phenomenon (Zhao et al, 1995;Sarens et al, 2021) is still unknown.…”