Abstract
During meiosis, most organisms ensure that homologous chromosomes undergo at least one exchange of DNA, or crossover, to link chromosomes together and accomplish proper segregation. How each chromosome receives a minimum of one crossover is unknown. During early meiosis in Caenorhabditis elegans and many other species, chromosomes adopt a polarized organization within the nucleus, which normally disappears upon completion of homolog synapsis. Mutations that impair synapsis even between a single pair of chromosomes in C. elegans delay this nuclear reorganization. We quantified this delay by developing a classification scheme for discrete stages of meiosis. Immunofluorescence localization of RAD-51 protein revealed that delayed meiotic cells also contained persistent recombination intermediates. Through genetic analysis, we found that this cytological delay in meiotic progression requires double-strand breaks and the function of the crossover-promoting heteroduplex HIM-14 (Msh4) and MSH-5. Failure of X chromosome synapsis also resulted in impaired crossover control on autosomes, which may result from greater numbers and persistence of recombination intermediates in the delayed nuclei. We conclude that maturation of recombination events on chromosomes promotes meiotic progression, and is coupled to the regulation of crossover number and placement. Our results have broad implications for the interpretation of meiotic mutants, as we have shown that asynapsis of a single chromosome pair can exert global effects on meiotic progression and recombination frequency.
Highlights
Meiosis ensures the reductional division of a diploid genome into haploid complements
Previous work has documented the appearance of nuclei in the premeiotic germline and the ‘‘transition zone,’’ which corresponds to the stages of leptotene and zygotene, where pairing and synapsis are initiated
We have shown that the failure of a single pair of chromosomes to synapse during meiotic prophase has farreaching effects on the other chromosomes in the nucleus
Summary
Meiosis ensures the reductional division of a diploid genome into haploid complements. Proper meiotic segregation depends on pairing, synapsis, and crossing over between homologous chromosomes. In addition to promoting genetic diversity [1,2], crossing over enables the bi-orientation of homologs at metaphase I by establishing physical connections (chiasmata) between chromosomes [3]. Crossover recombination is essential for proper meiotic chromosome disjunction. The very low frequency of achiasmate chromosomes at metaphase I implies that a specific mechanism ensures the placement of at least one crossover per chromosome, called the ‘‘obligate crossover.’’ In principle, a minimum crossover number of one could be achieved with an unregulated, random process, if the number of crossovers was sufficiently high. Most organisms have far too few crossovers for a Poisson process to ensure that each chromosome receives at least one [4]
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