Human meiosis II. Chromosome pairing and recombination nodules in human spermatocytes

Abstract

Meiosis in human spermatocytes has been analyzed by three dimensional reconstructions of 4 leptotene, 4 earlymid zygotene, 10 late zygotene, and 21 early pachytene nuclei. At leptotene, a lateral component is organized along each chromosome and the telomeres attach to the nuclear envelope. At early zygotene, the attachment sites aggregate and a chromosome bouquet is formed. Pairing and synaptonemal complex formation are initiated from the telomeres by binding of precursor material for the central region to the lateral components of the aligned homologues. In the 10 late zygotene nuclei, on the average 72% of the autosomal complement had been paired. Synaptonemal complex formation is in most cases initiated from both ends of the homologues and only in 5 cases was initiation of complex formation interstitial. Pairing of the short arms of the acrocentric bivalents and the X and Y chromosomes is delayed compared to the remainder of the genome. Irregularities such as interlockings and breaks of the lateral components of chromosomes or breaks of the synaptonemal complexes of bivalents are observed in 8 out of the 10 nuclei. Most of the breaks appeared to be the result of a resolution of interlockings. At early pachytene, all bivalents are fully paired the only exception being the secondary constrictions on bivalents 1 and 9 which frequently remain unpaired. In all nuclei, a short stretch of synaptonemal complex is present between the X and Y chromosomes. Only two interlockings and three breaks of lateral components of chromosomes were found at this stage. Recombination nodules are present in or at the central region of the synaptonemal complex from early zygotene and evidence has been obtained in favor of an attachment of nodules to precursor material for the central region at the pairing fork. Nodules can, however, also attach to a fully formed synaptonemal complex. At late zygotene, an average number of 101 nodules per nucleus is present. Assuming that all regions of the complex have equal probabilities of receiving a nodule about 144 nodules are expected to be present at the moment of complete pairing. At early pachytene, the mean number of nodules is 75. Generally, nodules appear to be distributed evenly along the bivalent arms. Nodules are present, however, in excess in the telomere regions and in the XY bivalent while the centromere regions, the secondary constrictions, and the short arms of the acroeentric bivalents are relatively depleted of nodules. Measurements of the distances between adjacent nodules and a comparison with a theoretical distribution of such distances assuming a random positioning of nodules have demonstrated that at late zygotene nodules are more frequently clustered than would be expected if they were distributed independently. At early pachytene, the reverse pattern is observed.

Chromosome pairing in autotetraploid Bombyx females. Mechanism for exclusive bivalent formation

“…The very high frequency of quadrivalents involving chromosomes 1 and the fact that the switch of pairing partner in most cases occurs within the knob furthermore indicates that the knob impedes synaptonemal complex formation promoting initiation from both ends of the chromosomes. A similar effect of condensed chromatin has been noted in human spermatocytes (25) where the rate of synaptonemal complex formation is retarded in the centromere region while in the secondary constrictions of bivalents 1, 9 and 16 synaptonemal complex formation is delayed until mid pachytene.…”

“…A recent analysis of chromosome pairing and synaptonemal complex formation in human spermatocytes heterozygous for a reciprocal translocation (14,25) likewise demonstrated a homologous phase of pairing at zygotene followed by a nonhomologous phase of pairing at mid-pachytene. The pairing of the involved segments was in all early pachytene nuclei strictly homologous resulting in the formation of a quadrivalent whereas at mid-late pachytene, one of the four nuclei analyzed revealed extensive nonlaomologous pairing of the involved chromosomes and their homologues.…”

“…It has therefore been proposed (24,26) that in the absence of stabilizing crossovers in the region between the interlocked segment and the nuclear envelope, interlockings can resolve by dissolution of the synaptonemal complex, movement of the interlocked lateral component or bivalent relative to the interlocking bivalent followed by a reformation of the synaptonemal complex. If the pairing is stabilized by crossovers, interlockings have to be resolved by breakage and reunion of lateral components or synaptonemal complexes as indeed is observed in human spermatocytes (25): At late zygotene 60 % of the nuclei contained one or more interlockings whereas only 4.8 % did so at early pachytene. At late zygotene, several breaks of lateral components or synaptonemal complexes could be identified.…”

“…Evidence from di-and triploid Bombyx females (22,24) as well as from other organisms (12,14,25,33) have demonstrated that chromosome pairing during zygotene is exclusively confined to homologous regions. In tetraploid Bombyx females, the distinction between homologous and non_homo-logous pairing is hampered by the fact that only chromosomes 1 and 2 can be identified with certainty.…”

Chromosome pairing in triticum aestivum cv. Chinese Spring

“…The serial sections were examined in a Siemens Elmiskop 102 electron microscope at 80kV and micrographs of selected nuclei were taken at a primary magnification of 3000 times and printed to a final magnification of between 14,700 and 21,000 times. Three dimensional reconstructions of the lateral components, together with the length measurements were performed as described by RASMUSSEN and HOLM (11). In the present study, 17 nuclei were serially sectioned and photographed (119 to 194 sections per nucleus) and the chromosomes of one early zygotene nucleus were fully traced onto transparent plastic (Figure 13).…”