Meiotic chromosome pairing in the fission yeast S. pombe

Meiosis is the cell division which gives rise to haploid gametes. During meiosis corresponding parental chromosomes pair in order to ensure their recombination and regular disjunction. The synaptonemal complex (SC) is a highly conserved structure in cells undergoing meiosis. Despite its well known ultrastructure and chemical composition, its functions are still under debate. Recombination, chromosome condensation and cohesion rely on factors whose homology to prokaryotic proteins suggest that the functions of recombination/recombinational repair and structural organization/compaction of chromosomal material are ancient functions that have been recruited for use with meiosis. However, no such homologies have been identified for components with a role in synapsis. This suggests that synapsis is a novel accession and only of minor importance for core meiotic functions like homology recognition and exchange. And yet the synaptonemal complex must have a function that outweights the cost of the formation of such an elaborate structure, as it is shared by the vast majority of sexually reproducing eukaryotes. The linear elements of the fission yeast, Schizosaccharomyces pombe may be evolutionary relics of SCs and represent the minimum structural requirement to ensure chiasmatic meiosis or they may just be rudiments deprived of any function. The existence of several mutants in which they are lacking and in which meiosis is impaired, suggests that they serve a role in meiosis. Here, we want to study the composition of linear elements to see which phylogenetic relationship exists to components of the synaptonemal complex. We also plan to study the temporal and spatial relationship of the linear elements to molecular recombination and homologous pairing. Information on the composition and function of linear elements will help to determine the structural requirements for meiosis- (and also partially mitosis-) related processes like chromosome condensation, sister chromatid cohesion, chromosome pairing and recombination.

The synaptonemal complex (SC) is a highly conserved structure in cells at meiosis. It mediates the pairing of homologous chromosomes and is important for the exchange of chromosome parts that leads to genetic recombination. Furthermore, the pairing of chromosomes is important for their subsequent sgregation to germ cells. The fission yeast Schizosaccharomyces pombe does not form SCs in meiotic prophase nuclei. Instead, thin threads, the so-called linear elements (LEs), are observed at the corresponding stages by electron microscopy. In this project we were studying the composition of LEs and their temporal and spatial relationship to molecular recombination and homologous pairing. We demonstrated that S. pombe Rec10 is a protein related to the Saccharomyces cerevisiae SC protein Red1 and that it localizes to LEs. Moreover, a homolog of S. cerevisiae Hop1 does exist in S. pombe and we showed by in situ immunostaining that it, as well as the kinase Mek1 (a homolog of which is also known to be associated with SCs), localizes to LEs. These observations indicate the evolutionary relationship of LEs with the lateral elements of SCs and suggest that these structures may exert similar functions in S. cerevisiae and S. pombe (Lorenz et al., 2004). It is known that Rec10 is essential for meiotic recombination, which raises the question as to whether a spatial relationship between recombination sites and LEs exists. We used immunocytology to demonstrate that Rec7 and Rad51, proteins that are involved in the formation and processing of meiotic DNA double-stranded breaks, localize to LEs. This led us to propose that LEs have the function to recruit recombination proteins to designated recombination sites on the chromosomes.