Plant chromosome homology: hypotheses relating rendezvous, recognition and reciprocal exchange

Abstract

Many higher eukaryotes have dispersed repetitive DNA and multiple instances of segmental duplications. As well, many plants and lower animals are polyploids. Thus restricting reciprocal genetic exchange to truly homologous chromosomes is likely a multi-step process. We propose the following sequence of events. First the ability to form a synaptonemal complex (SC) prematurely (i.e. before homology checking/recognition) is precluded by the organization of chromosomes during premeiotic S phase. Next rough alignment is accomplished regionally by having key allelic transcription units brought to the same transcription center. Once rough alignment is accomplished, close alignment can occur in conjunction with homology checking/recognition. Successful homology checking produces changes that now permit SC formation within the region of the check. Some organisms (with challenges to true homology such as dispersed repetitive DNA and segmental duplications) may require that, for a region to be competent to form an SC, successful homology checks must occur at both ends of the region. Successful early SC formation may provide an environment in which recombination intermediates can be earmarked for resolution into crossovers. Later in prophase I SC formation can occur nonhomologously, if two unsynapsed chromosomal axes meet.

Homologues of potato chromosome 5 show variable collinearity in the euchromatin, but dramatic absence of sequence similarity in the pericentromeric heterochromatin

“…However, in many organisms homologous pairing has been found to be independent of recombination [45], as must be partially the case also in potato, where genetic recombination is repressed in the heterochromatin [21,29]. Alternatively, it has been proposed that the rough alignment of the synaptonemal complex depends on bringing together key allelic transcription units [48]. …”

Centromere Associations in Meiotic Chromosome Pairing

“…The RNA-binding proteins Mei2 and Mmi1 form foci at the sme2 locus, and Mmi1 negatively regulates pairing (41), implicating both DNA-RNA and RNA-protein interactions in this process. To date, there is no clear evidence to support the notion that RNA transcripts may mediate homologous chromosome pairing in other organisms, but meiotic-specific RNA transcripts distributed over each homolog could assist in the homology search and pairing processes (62,137,139). An intriguing hypothesis is that centromeric and possibly heterochromatic regions in general could represent such sites.…”

From early homologue recognition to synaptonemal complex formation

“…Involvement of allelic transcription units is also suggested for pairing in polyploids (Wilson et al 2005). (3) High-resolution cytology on GFP-tagged loci of living Drosophila cells showed that homologous interactions correspond to random, diffuse walk motion.…”