Human meiosis VI. Crossing over in human spermatocytes

Abstract

The structure, number and distribution of recombination nodules in human spermatocytes have been analyzed by serial sectioning and three dimensional reconstruction of 10 late zygotene and 73 pachytene nuclei, the pachytene nuclei being allocated to seven substages. The analysis has permitted the following observations and conclusions. 1) Recombination nodules bind to the central region of the synaptonemal complex at zygotene, increase in size and transform, at pachytene stage 2, into a bridge-like structure termed a bar. During pachytene stages 3 and 4, the bars become more spindle shaped and are often oriented obliquely to the synaptonemal complex. By pachytene stages 5–7 the bars appear to resolve into filaments and disappear eventually. 2) The number of nodules decreases from a mean of 101 at late zygotene (72 percent pairing) to 75 at pachytene stage 1. At pachytene stage 2, 58 nodules and 16 bars are present, the corresponding figures for pachytene stages 3, 4 and 5 being 11 and 35, 6 and 35 and 7 and 24. At the later stages very few nodules and bars are seen. 3) Nodules are distributed at random among the bivalents and the bivalent arms at zygotene while at pachytene stage 3+4, 99 percent of the bivalents and 75 percent of the bivalent arms have at least one nodule or bar. By stage 5 the nodulebar distribution is to a large extent random. 4) The structural, numerical and distributional changes of nodules and bars suggest that the transformation of a nodule into a bar reflects a crossing over event. 5) As not all crossovers of a nucleus can be observed at the same time, the total crossover distribution was constructed by cumulating the frequencies of bars at stage 2 and the nodules and bars at stage 3–7. The frequency of crossing over is high in the distal segments and low near the centromeres. In longer bivalent arms crossing over is also frequent in one or more interstitial segments. Crossing over occurs in 75 percent of the XY bivalents as judged by the frequency of nodules in the synaptonemal complex which combines the homologous regions of the X and Y chromosomes. 6) The total number of crossovers is estimated to range from 69 to 73 per nucleus and compares with a mean of 50 chiasmata at diakinesis. 7) The distribution of chiasmata at diakinesis and that of crossovers at pachytene differs, especially in the short arms. 8) One crossover (rarely two) in the form of a recombination structure is present in the short bivalent arms. Several crossovers are present in the longer arms, but preferentially placed in the middle of two or three domains. Once a crossover has occurred in a domain, the probability for a second crossover to be realized in the same domain is decreased. The limitation to the placement of a single crossover in a short arm and in a domain of a long arm is a source for positive interference in genetic linkage analyses.