▪ Abstract Meiotic chromosomes have been studied for many years, in part because of the fundamental life processes they represent, but also because meiosis involves the formation of homolog pairs, ...

Meiotic chromosomes: integrating structure and function.

Over the last three decades, mitochondrial DNA has been the most popular marker of molecular diversity, for a combination of technical ease-of-use considerations, and supposed biological and evolutionary properties of clonality, near-neutrality and clock-like nature of its substitution rate. Reviewing recent literature on the subject, we argue that mitochondrial DNA is not always clonal, far from neutrally evolving and certainly not clock-like, questioning its relevance as a witness of recent species and population history. We critically evaluate the usage of mitochondrial DNA for species delineation and identification. Finally, we note the great potential of accumulating mtDNA data for evolutionary and functional analysis of the mitochondrial genome.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-294X.2009.04380.x

Mitochondrial DNA as a marker of molecular diversity: a reappraisal

In Saccharomyces cerevisiae, meiotic recombination is initiated by Spo11-dependent double-strand breaks (DSBs), a process that precedes homologous synapsis. Here we use an antibody specific for a phosphorylated histone (gamma-H2AX, which marks the sites of DSBs) to investigate the timing, distribution and Spo11-dependence of meiotic DSBs in the mouse. We show that, as in yeast, recombination in the mouse is initiated by Spo11-dependent DSBs that form during leptotene. Loss of gamma-H2AX staining (which in irradiated somatic cells is temporally linked with DSB repair) is temporally and spatially correlated with synapsis, even when this synapsis is 'non-homologous'.

Recombinational DNA double-strand breaks in mice precede synapsis

In nearly all eukaryotes, at least some individuals inherit mitochondrial and chloroplast genes from only one parent. There is no single mechanism of uniparental inheritance: organelle gene inheritance is blocked by a variety of mechanisms and at different stages of reproduction in different species. Frequent changes in the pattern of organelle gene inheritance during evolution suggest that it is subject to varying selective pressures. Organelle genes often fail to recombine even when inherited biparentally; consequently, their inheritance is asexual. Sexual reproduction is apparently less important for genes in organelles than for nuclear genes, probably because there are fewer of them. As a result organelle sex can be lost because of selection for special reproductive features such as oogamy or because uniparental inheritance reduces the spread of cytoplasmic parasites and selfish organelle DNA.

https://www.pnas.org/content/pnas/92/25/11331.full.pdf

Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution.

Mice that are deficient in either the Pms2 or Msh2 DNA mismatch repair genes have microsatellite instability and a predisposition to tumours. Interestingly, Pms2–deficient males display sterility associated with abnormal chromosome pairing in meiosis. Here mice deficient in another mismatch repair gene, Mlh1, possess not only microsatellite instability but are also infertile (both males and females). Mlh 1 –deficient spermatocytes exhibit high levels of prematurely separated chromosomes and arrest in first division meiosis. We also show that Mlh1 appears to localize to sites of crossing over on meiotic chromosomes/Together these findings suggest that Mlh1 is involved in DNA mismatch repair and meiotic crossing over.

Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over.

Using the Counce-Meyer spreading technique, in over 70 spermatocytes it was possible consistently to obtain whole, flattened nuclei containing complete sets of pachytene SCs. The SCs are visible in both the phase and electron microscopes. Each SC is morphologically intact, preferentially stained, and attached to the nuclear envelope by a dense, terminal plaque. It is thus possible to trace each SC for its entire length. Also, a structure representing the kinetochore is clearly visible in each autosomal SC. Karyotypes comparable to the somatic karyotype can be constructed by arranging SCs according to length and kinetochore position. The observed regularity of SC morphology implies structural stability sufficient to withstand the stresses imposed by the procedure.— A coarse network of closely packed nuclear annuli connecting SC attachment plaques often provides end-to-end associations and may tend to immobilize SCs during processing.— Three kinds of perturbation of SC structure are encountered. Twists in the SC frequently occur, but no regular pattern or correspondence with chiasma distribution is observed. SCs occasionally hook around each other without disruption, but in two instances the unpaired axis of the X apparently was interlocked within an autosomal SC. Stretching of the SC is infrequent; it is conspicuous when it occurs and is usually associated with other obvious distortions of the nucleus.— Distinctive morphologies of the X and Y chromosomes facilitate their identification in all preparations. — During zygotene, autosomal synapsis, i.e., the formation of SCs from the pairing of single axial elements, initiates at distal ends and terminates at the kinetochore region; neither initiation nor termination is synchronous among all autosomes.

Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). I. Morphology of the autosomal complement in spread preparations.

Surface spread spermatocytes of mice heterozygous for a tandem duplication show nuclei in late zygotene-early pachytene in which the heteromorphic synaptonemal complex (SC) contains a lateral element that is buckled out into an unpaired loop as a consequence of the added length of the duplication (estimated in another study to be 21.7%, with breakpoints at 0.50 and 0.72 of the length of the chromosome). The ends of the buckle, marking the interstitial termini of synapsis proceeding from opposite directions, vary over a wide range of positions, but within limits: the proximal end of the loop does not exceed the distal end of the duplication segment, while the distal end of the loop does not lie closer to the kinetochore than the proximal end of the segment. Thus, synapsis (SC formation) at zygotene is restricted to homologous regions (exclusive homosynapsis). — In the last half of pachytene, no buckles are found, only simple SCs with lateral elements of equal length, as a consequence of synaptic adjustment. Intermediate stages of adjustment are found throughout the first half of pachytene. Shortly after homosynapsis is complete, synaptic adjustment begins: the ends of the duplication loop separate (desynapsis of homosynapsed regions); the long axis shortens with respect to the short axis in both the unpaired loop and in the SC portions; asymmetrical twists take up inequalities; the loop is reduced to from 1 to 3 asymmetrical twists; the axes (lateral elements) equalize as the long axis shortens; and a simple SC is formed, indistinguishable from others in the complement, in which the region of the duplication and those adjacent to it have heterosynapsed, while the distal regions of the SC are presumably still homosynapsed. Synaptic adjustment evidently involves two sequential events: localized instability of the homosynapsed condition, leading to desynapsis, then restoration of the SC by heterosynapsis. Adjustment therefore represents the loss of strict homosynapsis. It is concluded that the asymmetry produced by the duplication loop constitutes an instability that triggers synaptic adjustment.

Synaptonemal complex analysis of mouse chromosomal rearrangements. I. Cytogenetic observations on a tandem duplication.

Human pachytene chromosome pairs have been characterized electron microscopically in spread preparations on the basis of synaptonemal complex length, kinetochore position and attached nucleoli when present. The X and Y chromosomes can be followed by their filamentous axial cores from partial synapsis, through precocious disjuction and end-to-end attachment, to differentiation of a network in the sex chromosome pair.

https://science.sciencemag.org/content/sci/187/4174/363.full.pdf

Synaptonemal complex complement of man in spreads of spermatocytes, with details of the sex chromosome pair

The sperm of the crayfish, Procambarus clarkii, is relatively simple among decapod sperm and was described in the first paper of this series (28). The present paper details the development of this sperm as followed with the light and electron microscopes. The process is divided into six stages for purposes of description. The main points of interest discussed are the absence of mitochondria or mitochondrial derivatives in the mature sperm, the development of a complex acrosome in the absence of highly organized characteristic Golgi apparatus but in the presence of small stacks of annulate lamellae, and the changes in the nucleus. Of the latter, the elaborate convoluted sheets of membrane that are extensions of the nuclear envelope are unique. The nucleus undergoes unusual changes in size and shape that are accompanied by several phases of organization of the chromatin. In the mature sperm the nucleus is empty-appearing and notably lacking in any apparent high degree of order. The entire development of the sperm is consonant with the idea that the fate of the mitochondria and centrioles, structures that figure prominently in the elaborate architecture of flagellate sperm, is associated with the lack of a flagellum.

/pdf/spermiogenesis-in-the-crayfish-procambarus-clarkii-ii-1uooay9pvn.pdf

SPERMIOGENESIS IN THE CRAYFISH (PROCAMBARUS CLARKII) : II. Description of Stages

The X and Y chromosome axes have a distinctive morphology at pachytene and are clearly distinguishable from autosomal SCs. The X and Y are totally unpaired at late zygotene when most of the autosomes are synapsed; however, their attachment points at the presumptive SC end are closely apposed. The X and Y axes pair to form a length of SC that is somewhat shorter than the unpaired portion of the Y. Unpaired axes may appear thin and sometimes double, or may thicken to form fusiform bulges that are sometimes hollow: two on the X and one on the Y. Discrete differentiations, tentatively identified as kinetochores, are often visible at the proximal end of the SC on the Y axis, and also between the fusiform differentiations on the X axis. Additional differentiations, in the form of loops and densely staining granular excrescences form on the X axis and sometimes on the Y. A further differentiation appears as a cloud-like sheath around the distal end of the X axis, often in association with a bi-lobed dense body. At late pachytene, the XY-SC remains intact, but the unpaired X and Y axes develop side branches. Just before diplotene, while the autosomal SCs are still intact, the XY-SC is lost, although the axes persist and remain together at the attachment point of the SC. The X and Y differentiations form a logical temporal sequence when grouped according to progressive structural complexity. The morphological types may serve as markers for the sub-stages of pachytene.

Montrose J. Moses

Papers

Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). I. Morphology of the autosomal complement in spread preparations.

Synaptonemal complex analysis of mouse chromosomal rearrangements. I. Cytogenetic observations on a tandem duplication.

Synaptonemal complex complement of man in spreads of spermatocytes, with details of the sex chromosome pair

SPERMIOGENESIS IN THE CRAYFISH (PROCAMBARUS CLARKII) : II. Description of Stages

Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). II. Morphology of the XY pair in spread preparations.