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Meiotic chromosome pairing and recombination

 

Principal Investigator: Josef Loidl

Cells of sexually reproducing eukaryotes normally contain two equal (homologous) sets of chromosomes, one contributed by the father, the other by the mother during the fusion of gametes and the formation of a zygote. When eggs or sperm are produced, they must be endowed with a single set of chromosomes. Therefore, germ progenitor cells undergo a reductional division, meiosis. During meiosis, homologous chromosomes of paternal and maternal origin juxtapose and become connected by a protein structure, the synaptonemal complex (SC). They then exchange parts and segregate to different daughter nuclei. Thus, the function of meiosis is twofold – it compensates for the doubling of the chromosome number at fertilization and it provides the progeny with newly assorted sets of alleles, which is the basis of their genetic heterogeneity. Failures in meiosis may lead to gametes with aberrant chromosome numbers and thus to progeny with congenital defects.

A pair of mating Tetrahymena cells undergoing simultanous meioses. The meiosis-specific recombination protein Dmc1 (yellow) is exclusively expressed in the generative micronuclei which, at meiotic prophase, are crescent-shaped. The related nonspecific recombination protein Rad51 (magenta), while being essential for meiotic DSB repair, localizes primarily to the non-meiotic macronuclei (cyan).

Recombination proteins in Tetrahym ena. A pair of mating Tetrahymena cells undergoing simultanous meioses. The meiosis-specific re c ombination protein Dmc1 (yellow) is exclusively expressed in the generative micronuclei which, at meiotic prophase, are crescent-shaped. The related nonspecific recombination protein Rad51 (magenta), while being essential for meiotic DSB repair, localizes primarily to the non-meiotic macronuclei (cyan).

We are studying various aspects of meiotic chromosome organisation and behaviour in evolutionarily divergent organisms such as yeasts and ciliates, to learn which adaptations and amendments have occurred during the evolution of extant meiosis.
In particular, we are investigating meiotic chromosome pairing and recombination in the fission yeast and in the ciliate Tetrahymena, which have both lost their SC. In the fission yeast, we identified chromosome axis-associated protein structures that appear to represent evolutionary relics of SCs. We found that Spo11(Rec12), the factor that elicits recombination by inducing DNA double-strand breaks (DSBs), is targeted to chromatin by these proteins. In Tetrahymena, Spo11-dependent DSBs cause an enormous elongation of meiotic nuclei. The ensuing close parallel and polarized arrangement of chromosomes within the tubular nucleus, which is reminiscent of the conserved bouquet organization, promotes homologous pairing and recombination. A similar, although less pronounced, change in nuclear shape is observed in the fission yeast. Thus, this adaptation may have evolved to compensate for the lack of an SC. Moreover, in these two organisms, the absence of the SC may have led to a non-canonical processing of meiotic recombination intermediates involving the Mus81 nuclease, which constitutes only a minor recombination pathway in the majority of eukaryotes.
Ultimately, our studies will help to understand the origin and function of conserved meiotic features such as the SCs, the chromosomal bouquet, and the regulation of meiotic recombination.

 

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