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.

Highlights

  • Meiosis is a specialized cell division that reduces ploidy by half and generates cells essential for sexual reproduction. It consists of a single round of pre-meiotic DNA replication, followed by two consecutive rounds of chromosome segregation, in which homologous chromosomes separate in meiosis I, and sister chromatids separate in meiosis II, to yield four daughter cells

  • Meiotic recombination occurs during prophase I and involves pairing and synapsis of homologous chromosomes, followed by the reciprocal exchange of genetic information via crossovers (COs), which are cytologically manifested as chiasmata (Janssens, 1909; Hunter, 2015)

  • Consistent with this, quantitative determination of Chromatid interference (CI) across the genome and for all individual chromosomes yields CI values that do not significantly differ from 0 (Table 1 and Supplementary Table 2). These findings demonstrate that Arabidopsis male meiosis does not experience any bias toward a specific DCO type on a genome-wide or chromosome-specific level

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Summary

Introduction

Meiosis is a specialized cell division that reduces ploidy by half and generates cells essential for sexual reproduction. Prior CI analyses are limited to accepting or rejecting a fit to the expected 1:2:1 ratio and are mainly focused on genome-wide effects, leaving many questions unanswered, including: “If CI is present, does it show variation in strength across chromosomes?,” “Is CI subject to chromosome-specific or location-specific effects?,” “Does inter-CO distance influence CI and is there a link with CO interference?,” and “Does CI differ between male and female meiosis?.” In this study, we introduce a novel analytical framework for the quantitative interpretation of CI and apply this to tetrad-based genotyping data from Arabidopsis and maize male meiosis to unravel putative, yet unexplored CI effects.

Results
Conclusion

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