Presynaptic events in meiocytes of Lilium longiflorum and their relation to crossing-over: a preselection hypothesis.

Abstract

We are proposing a "Preselection Hypothesis" to account for the regulation of crossing-over in eukaryotic organisms. The hypothesis characterizes meiosis in terms of three major physiological stages: (1) a presynaptic stage when pairs of homologous DNA stretches are selected so as to become trapped within the synaptinemal complex during synapsis, (2) an alignment of homologous chromosomes and stabilization of paired bivalents via the synaptinemal complex, and (3) a scission and rejoining of DNA stretches leading to the formation of chiasmata and crossovers. The hypothesis centers on the first stage and is based on evidence for the occurrence of significant cytological and biochemical changes prior to synapsis. The major feature of the hypothesis is that crossing-over occurs only in trapped DNA stretches. Thus, potential crossing-over sites, though not crossingover itself, are determined well before chromosomes pair. Since, to a large degree, crossovers are distributed randomly along the length of each chromosome, the preselection process must result in a random assortment of trapped DNA stretches, the assortment differing from one meiocyte to another.The principal challenge in explaining crossing-over in eukaryotes is not so much the molecular mechanism of exchange between DNA strands as the mode of organization by which these exchanges are regularly effected in meiotic cells. Although prokaryotes provide a system of choice for probing the immediate events of DNA recombination, eukaryotes house facilitating mechanisms that are superimposed on the pure process of molecular recombination. The juxtapositioning of homologous chromosomes whose DNA lengths may exceed one meter, the apparent exclusion of sister-chromatid exchanges in the face of closely aligned sisters and homologs, the organization of homologous chromatids to accommodate four-strand crossing-over, the regulated distribution of exchanges as manifested in positive interference, and the restriction of the total process to differentiated meiocytes are specific items in the complex calendar of events governing meiotic recombination in eukaryotes. ConsiderationsAlthough some uncertainty exists about the precise time at which strand exchanges occur in relation to the formation of the synaptinemal complex (SC), there can be little doubt that DNA strands transverse the complex at crossover sites. Unless crossing-over precedes synapsis, a possibility that we summarily set aside, its occurrence must be restricted to situations in which homologous regions are closely juxtaposed Abbreviation: SC, synaptinemal complex. within the SC. Such situations, however, would only allow for a very small proportion of DNA to engage in crossing-over. This follows from the morphology of the pachytene bivalent. Generally, "the SC joins homologous chromosomes over their whole length" (1). However, in the three species so far analyzed, namely Neurospora crassa (2), Drosophila melanogaster (3), and Zea mays (4), the length ratios of SC to chromosome DNA were about 0.3%, 0.2%...

Sex difference in recombination frequency in Arabidopsis

“…2 2 Proceeding from the hypothesis of the possible connection between the state of a chromosome region in the germ cell line and the probability of its involvement in the crossing over process (Stern et aL, 1975;Korol, 1983, 1985), we expect that the nitrate ion treatments will result in changes of recombination between marker loci flanking chl-2. It is this result that has been established in the analysis of treatment consequences based on estimation of rf (table 2).…”

Effective chromosome pairing requires chromatin remodeling at the onset of meiosis

“…On entry into meiosis just before chromosome pairing, the subtelomeric heterochromatin knobs visualized on Lilium, rye, and maize chromosomes ''disappear'' as a result of these conformational changes (3)(4)(5)(6). In common with these structural changes in the subtelomeric regions, visualization of the overall chromosome structure by using dispersed repetitive sequences reveals that these repetitive regions also undergo extensive remodeling before pairing (7).…”

The premeiotic DNA replication of euchromatin and heterochromatin in Lilium longiflorum (Thunb.)

“…A morphological description of the presynaptic stages in Lilium has been given by STERN, WESTERGAARD & VON WETTSTEIN (65). The autoradiographical data necessitate a minor extension of the terminology.…”

“…The chromatin has been reported to undergo compaction before the leptotene stage (5,6,74,75) similar to the situation in other organisms (10,25). During the presynaptic interval in Lilium a succession of stages is identifiable by distinctive changes in the organization of the heteroehromatin and the nucleoli, and it has been suggested that the premeiotic heterochromatin might have an impact on the control of the crossing-over process (65).…”