The Relation between the Axial Complex of Meiotic Prophase Chromosomes and Chromosome Pairing in a Salamander (Plethodon cinereus)

An investigation of the structure of meiotic chromosomes from primary spermatocytes of two salamanders, Plethodon cinereus and Desmognathus fusca, has been made using correlated light and electron microscopy. Feulgen squashes were compared with stained sections and these related to adjacent thin sections in the electron microscope. A transition from the familiar cytological preparation to the electron image was thus effected. A linear complex consisting of three parallel strands has been observed with the electron microscope, passing along the central axis of primary spermatocyte chromosomes. The complex is similar to that found in comparable chromosomes from at least a dozen animal species. The structure in Plethodon is described in detail. Synapsis has been positively identified as the stage of meiotic prophase at which the complex occurs. Thus the complex is a part of bivalent chromosomes. It has not been seen in other stages or other divisions and is thus thought to be exclusively of synaptic occurrence. The term synaptinemal complex is suggested for the entire structure. By virtue of the material condensed around it, the complex is also seen in the light microscope where it appears as a fine, densely Feulgen-positive central core along the chromosome. The complex is thus closely associated with DNA, if not at least in part, composed of it. In the stages studied, homologous chromosomes are not always completely paired. The lateral elements of the complex separate and follow the single chromosome axes at these points. The central element disappears and thus may be a phenomenon of pairing. It is concluded that the lateral elements of the synaptinemal complex may more correctly be a "core" of the single meiotic prophase chromosome, possibly being concerned with its linear organization.     

Synaptonemal Complex und Chromosomenstruktur in der achiasmatischen Spermatogenese vonPanorpa communis (Mecoptera)

Meiotic prophase in the spermatocytes ofPanorpa communis was studied. There is a proper sequence of meiotic stages in the testes. Therefore the temporal development of chromosome structure and the synaptonemal complex (SC) could be studied exactly. The structure and function of the SC are interpreted in a new model.—The chromosomes have a lambrush form from leptotene to diakinesis. At leptotene each chromatid produces an additional axis of basic protein and RNA. The axis becomes one of the lateral elements of the SC. At pachytene the DNA of the bivalents is separated into three regions: 1. Most of the DNA forms long loops outside the SC. 2. Smaller portions of the DNA filaments are twisted around the lateral elements of the SC. 3. Short DNA loops (called pairing loops) extend into the pairing space. InPanorpa the SC is composed of two lateral elements (chromosome axes), which are connected by equally spaced transverse filaments, a ladder-like central element in the middle of the pairing space and, on each side of the pairing space parallel to the lateral elements, two RNA containing strands. These are regarded as connected RNA copies of the pairing loops and are responsible for the exact pairing of homologous chromosome segments. At diplotene the axes of the sister chromatids separate to form “double complexes” with four lateral elements. The double complexes of the oocytes contain only transverse filaments between the axes of the homologous chromatids. After a short time they disappear again and the homologues separate to form the chiasmatic bivalents. In the spermatocytes all four chromatid axes are connected by transverse filaments. The pairing complex persists until diakinesis, thereby causing the suppression of the diplotene stage in the light microscope. This may be the only reason for the achiasmatic meiosis in the spermatocytes ofPanorpa.     

Maize meiotic mutants with improper or non-homologous synapsis due to problems in pairing or synaptonemal complex formation

During meiotic prophase homologous chromosomes find each other and pair. Then they synapse, as the linear protein core (axial element or lateral element) of each homologous chromosome is joined together by a transverse central element, forming the tripartite synaptonemal complex (SC). Ten uncloned Zea mays mutants in our collection were surveyed by transmission electron microscopy by making silver-stained spreads of SCs to identify mutants with non-homologous synapsis or improper synapsis. To analyse the mutants further, zyp1, the maize orthologue of the Arabidopsis central element component ZYP1 was cloned and an antibody was made against it. Using antibodies against ZYP1 and the lateral element components AFD1 and ASY1, it was found that most mutants form normal SCs but are defective in pairing. The large number of non-homologous synapsis mutants defective in pairing illustrates that synapsis and pairing can be uncoupled. Of the ten mutants studied, only dsy2 undergoes normal homologous chromosome recognition needed for homologous pairing. The dsy2 mutation fails to maintain the SC. ZYP1 elongation is blocked at zygotene, and only dots of ZYP1 are seen at prophase I. Another mutant, mei*N2415 showed incomplete but homologous synapsis and ASY1 and AFD1 have a normal distribution. Although installation of ZYP1 is initiated at zygotene, its progression is slowed down and not completed by pachytene in some cells and ZYP1 is not retained on pachytene chromosomes. The mutants described here are now available through the Maize Genetics Cooperation Stock Center (http://maizecoop.cropsci.uiuc.edu/).     

The meiotic prophase in Bombyx mori females analyzed by three-dimensional reconstructions of synaptonemal complexes

Serial sectioning followed by three dimensional reconstruction of lateral components of the synaptonemal complex have been used to follow chromosome pairing during the prophase of the achiasmatic meiotic division in the silkworm, Bombyx mori. During leptotene and early zygotene, the lateral components become attached to the nuclear envelope at a specific region, thus forming a chromosome bouquet. The attachment of lateral components to the nuclear envelope precedes the completion of the components between their attachment points. Synapsis and synaptonemal complex formation start during the period of lateral component organization in the individual nucleus. Telomeric movements on the nuclear envelope occur at two stages of the prophase: the chromosome pairing appears to be initiated by an association of unpaired ends of homologous chromosomes, the nature of this primary attraction and recognition being unknown. Secondly, the paired chromosomes become dispersed in the nucleus by shifting of attachment sites of completed synaptonemal complexes at the end of zygotene. This movement is possibly related to a membrane flow occurring during this stage. Membrane material is synthesized at the region of synaptonemal complex attachment. Later, the excess membrane material is shifted to the opposite pole where it protrudes into the lumen of the nuclei thus forming vacuoles. — Two previously undescribed features of chromosome pairing were revealed. In late zygotene, chromosome pairing and synaptonemal complex formation were frequently observed to be delayed or even prevented over a short distance by interlocking of two bivalents, both being attached to the nuclear envelope. Such interlocking of bivalents was not found in pachytene. Secondly, one nucleus was found in which two homologous chromosomes were totally unpaired while the remaining 27 bivalents were completed or in a progressed state of pairing. The lateral components of the two unpaired chromosomes had the same length and were located several microns apart, thus eliminating the possibility of a permanent association of homologous chromosomes before the onset of meiosis in Bombyx mori females. — During pachytene, one of the 8 cells belonging to the syncytial cell cluster characteristic of oogenesis continues the meiotic prophase whereas the remaining 7 cells, the nurse cells, enter a different developmental sequence, finally resulting in their degeneration. The synaptonemal complex of the oocyte develops into a sausage-like structure after pachytene by a deposition of dense material onto the lateral components, thus filling out most of the central region. The diameter of this modified synaptonemal complex reaches at least 300 nm, as compaired to a pachytene width of approximately 130 nm. Also, the length of synaptonemal complexes increases from 212 at zygotene/pachytene to at least 300 at the modified pachytene stage. In nurse cells, synaptonemal complexes are shed from the bivalents shortly after pachytene simultaneously with a condensation of the chromatin. These free synaptonemal complex fragments associate and form various aggregates, either more or less normal looking polycomplexes or various complex figures formed by reorganized synaptonemal complex subunits. Later stages have not been included in the present investigation.     

FINE STRUCTURE OF SYNAPSED CHOMOSOMES IN F1 LYCOPERSICON ESCULENTUM-SOLANUM LYCOPERSICOIDES AND ITS PARENTS

Typical synaptinemal complexes consisting of electron-dense central and lateral elements and much less dense outer fibrillar material are formed at meiotic prophase in Lycopersicon esculentum (tomato), Solanum lycopersicoides, their diploid hybrid, and occasionally in tomato haploids (in which an average of about one chromosome region per cell is synapsed nonhomologously). Complexes in the hybrid (in which the chromosomes synapse completely but often fail to form chiasmata) are similar to those in the parents. Complexes in the haploid are similar to those of diploid tomato. The data suggest that synaptinemal complexes form whenever chromosomes undergo meiotic synapsis, regardless of whether synapsis leads to chiasmata.     

The structure and function of the synaptinemal complex inLilium longiflorum sporocytes

The development of meiotic prophase in pollen mother cells ofLilium longiflorum is presented through photomicrographs of squashes and sections and through electron micrographs of thick and thin sections. Emphasis is placed on the first appearance of axial cores, the participation of axial cores in the formation of synaptinemal complexes, the fine structure of the complex and the fate of the complex at the end of pachytene. It is shown that axial cores are formed in early meiotic prophase chromosomes and that the two axial cores of a set of homologous chromosomes participate in the formation of a synaptinemal complex. It is proposed that the transverse filaments of each axial core meet and interdigitate and so produce the transverse filaments of the complex. It is shown that the complex is axial to the pachytene bivalent and that the association of the complex with chromosomal material is terminated at the end of pachytene. The pairing affinity of the cores in homologous and non-homologous chromosome associations is discussed. The zygotene stage is defined in terms of the occurrence of synaptinemal complexes and the attachment of the nucleolus to the nuclear membrane during this stage is noted.     

The fine structure of meiotic chromosome polarization and pairing in Locusta migratoria spermatocytes

At the leptotene stage of meiotic prophase in Locusta spermatocytes (2n=22 telocentric autosomes + X-chromosome), each chromosome forms an axial core. The 44 ends of the autosomal cores are all attached to the nuclear membrane in a small region opposite the two pairs of centrioles of the juxtanuclear mitochondrial mass. At later stages of meiotic prophase, the cores of homologous chromosomes synapse into synaptinemal complexes. Synapsis is initiated near the nuclear membrane, in the centromeric and the non-centromeric ends of the chromosomes. Homologous cores have their attachment points close together and some cores are co-aligned prior to synapsis. At subsequent stages of zygotene, the number of synaptinemal complexes at the membrane increases, while the number of unpaired axial cores diminishes. At pachytene, all 11 bivalents are attached to the membrane at both ends, so that there are 22 synaptinemal complexes at the membrane near the centrioles. Because each bivalent makes a complete loop, the configuration of the classic Bouquet stage is produced. The X-chromosome has a poorly defined single core at pachytene which also attaches to the nuclear membrane. These observations are based on consecutive serial sections (50 to 100) through the centriolar zone of the spermatocytes. Labeling experiments demonstrated that tritiated thymidine was incorporated in the chromatin of young spermatocytes prior to the formation of the axial cores at leptotene. It is concluded that premeiotic DNA synthesis is completed well in advance of pairing of homologous chromosomes, as marked by the formation of synaptinemal complexes.     

DNA AND THE FINE STRUCTURE OF SYNAPTIC CHROMOSOMES IN THE DOMESTIC ROOSTER (GALLUS DOMESTICUS)

The indium trichloride method of Watson and Aldridge (38) for staining nucleic acids for electron microscopy was employed to study the relationship of DNA to the structure of the synaptinemal complex in meiotic prophase chromosomes of the domestic rooster. The selectivity of the method was demonstrated in untreated and DNase-digested testis material by comparing the distribution of indium staining in the electron microscope to Feulgen staining and ultraviolet absorption in thicker sections seen with the light microscope. Following staining by indium, DNA was found mainly in the microfibril component of the synaptinemal complex. When DNA was known to have been removed from aldehyde-fixed material by digestion with DNase, indium stainability was also lost. However, staining of the digested material with non-selective heavy metal techniques demonstrated the presence of material other than DNA in the microfibrils and showed that little alteration in appearance of the chromosome resulted from DNA removal. The two dense lateral axial elements of the synaptinemal complex, but not the central one to any extent, also contained DNA, together with non-DNA material.     

Meiotic Exchange without the Synaptinemal Complex

THE synaptinemal complex is a ribbonlike tripartite structure, normally restricted to the nucleus of meiocytes and located along the longitudinal axis of bivalent chromosomes¹. It consists of two dense lateral elements (about 400 Å in width) separated from the central element (about 250 Å in width) by spaces of about 400 Å (Fig. 1). Various functions have been proposed for it, primarily that it is intimately involved in meiotic exchange, either directly by promoting effective pairing between complementary nucleotide strands of homologous chromosomes^1–3 or indirectly by providing for the rough alignment of homologues before their more intimate association^4,5. In this view, the complex is an essential feature of the regular and extensive exchange process typical of meiosis. The firmest evidence in support of its role in exchange has been its concomitant presence in primary meiocytes whenever genetic or cytological evidence indicates that crossing-over is occurring¹. The presence of the complex in meiocytes which lack exchange and/or chiasmata, for example, the female of Bombyx mori⁶, intergeneric hybrids, haploid genomes and certain achiasmate male insects, as well as its presence in univalent X chromosomes of primary spermatocytes and in postmeiotic spermatids, has been interpreted as “the exceptions that prove, or at least refine, the rule¹.” Here, for the first time, we describe the converse situation, one in which high frequencies of meiotic exchange, as determined by genetic tests, are not accompanied by a detectable synaptinemal complex. This means that both pairing of homologues, which must precede exchange and the exchange process itself can occur in the meiocyte without the aid of the synaptinemal complex.     

Differential distribution and association of repeat DNA sequences in the lateral element of the synaptonemal complex in rat spermatocytes

The synaptonemal complex (SC) is an evolutionarily conserved structure that mediates synapsis of homologous chromosomes during meiotic prophase I. Previous studies have established that the chromatin of homologous chromosomes is organized in loops that are attached to the lateral elements (LEs) of the SC. The characterization of the genomic sequences associated with LEs of the SC represents an important step toward understanding meiotic chromosome organization and function. To isolate these genomic sequences, we performed chromatin immunoprecipitation assays in rat spermatocytes using an antibody against SYCP3, a major structural component of the LEs of the SC. Our results demonstrated the reproducible and exclusive isolation of repeat deoxyribonucleic acid (DNA) sequences, in particular long interspersed elements, short interspersed elements, long terminal direct repeats, satellite, and simple repeats. The association of these repeat sequences to the LEs of the SC was confirmed by in situ hybridization of meiotic nuclei shown by both light and electron microscopy. Signals were also detected over the chromatin surrounding SCs and in small loops protruding from the lateral elements into the SC central region. We propose that genomic repeat DNA sequences play a key role in anchoring the chromosome to the protein scaffold of the SC. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes

Recent studies in simple model organisms have shown that centromere pairing is important for ensuring high-fidelity meiotic chromosome segregation. However, this process and the mechanisms regulating it in higher eukaryotes are unknown. Here we present the first detailed study of meiotic centromere pairing in mouse spermatogenesis and link it with key events of the G2/metaphase I transition. In mouse we observed no evidence of the persistent coupling of centromeres that has been observed in several model organisms. We do however find that telomeres associate in non-homologous pairs or small groups in B type spermatogonia and pre-leptotene spermatocytes, and this association is disrupted by deletion of the synaptonemal complex component SYCP3. Intriguingly, we found that, in mid prophase, chromosome synapsis is not initiated at centromeres, and centromeric regions are the last to pair in the zygotene-pachytene transition. In late prophase, we first identified the proteins that reside at paired centromeres. We found that components of the central and lateral element and transverse filaments of the synaptonemal complex are retained at paired centromeres after disassembly of the synaptonemal complex along diplotene chromosome arms. The absence of SYCP1 prevents centromere pairing in knockout mouse spermatocytes. The localization dynamics of SYCP1 and SYCP3 suggest that they play different roles in promoting homologous centromere pairing. SYCP1 remains only at paired centromeres coincident with the time at which some kinetochore proteins begin loading at centromeres, consistent with a role in assembly of meiosis-specific kinetochores. After removal of SYCP1 from centromeres, SYCP3 then accumulates at paired centromeres where it may promote bi-orientation of homologous centromeres. We propose that, in addition to their roles as synaptonemal complex components, SYCP1 and SYCP3 act at the centromeres to promote the establishment and/or maintenance of centromere pairing and, by doing so, improve the segregation fidelity of mammalian meiotic chromosomes.     

Synaptonemal complexes in insects

The synaptonemal complex (SC) is the key nuclear element formed in meiotic prophase I to join 2 homologous chromosomes at the pachytene bivalent. It is a highly conserved structure that is universally present in eukaryotes. The SC is presented as a tripartite protein structure, which consists of 2 lateral elements and a central region. In insects, the central region is particularly distinct and highly ordered. This made it possible to describe the fine structure of the central region and propose a model of its architecture. Chromatid DNA is arranged in chromatin loops extending radially from the SC. The loops appear to consist of a basic chromatin fiber with a diameter of 20–30 nm. In many insect species, synaptonemal polycomplexes occur in postpachytene cells. They represent one of the possible ways of SC degradation. Another process, which occurs beyond pachytene, is the formation of proteinaceous chromatid axis, the silver-stained chromatid core. Based on results in insect models, the chromatid cores have been related to the structure and formation of the SC. Research on insect models significantly contributed to understanding individual steps of the SC formation and temporal sequence of chromosome pairing. These include the formation of lateral elements of the SC, pairing initiation, interlocking of chromosomes, and synapsis of homologous chromosomes. Attention is also given to non-homologous pairing, including synaptic adjustment, correction of pairing, and pairing of sex chromosomes. In the next section, chiasmatic and achiasmatic modes of meiosis are compared with respect to the SC formation. In the chiasmatic mode, the SCs display recombination nodules that are believed to mediate the process of recombination. These nodules were discovered in insects, and indirect evidence for their role comes from insects. Two different examples of achiasmatic meiosis, occurring in the heterogametic sex of several insect orders, are given: one involves the SC formation, whereas in the other, SCs are absent. Finally, the potential of SC karyotyping for analysis of the insect genome is discussed.     

Coordinating the events of the meiotic prophase

Meiosis is a specialized type of cell division leading to the production of gametes. During meiotic prophase I, homologous chromosomes interact with each other and form bivalents (pairs of homologous chromosomes). Three major meiotic processes--chromosome pairing, synapsis and recombination--are involved in the formation of bivalents. Many recent reports have uncovered complex networks of interactions between these processes. Chromosome pairing is largely dependent on the initiation and progression of recombination in fungi, mammals and plants, but not in Caenorhabditis elegans or Drosophila. Synapsis and recombination are also tightly linked. Understanding the coordination between chromosome pairing, synapsis and recombination lends insight into many poorly explained aspects of meiosis, such as the nature of chromosome homology recognition.     

Whole mount electron microscopy of meiotic chromosomes and the synaptonemal complex

The mechanism by which homologous chromosomes pair and crossover has been a major unsolved problem in genetics. Thin section electron microscopy of the synaptonemal complex has not provided enough details to allow any significant insight into this problem. Whole mount preparations of the testis of mice, quail, crayfish, and frogs provided a striking improvement in visualization of the morphological features of meiotic chromosomes. These studies, when combined with the use of deoxyribonuclease and trypsin allowed the following conclusions. 1. The synaptonemal complex (lateral and central elements with connecting L-C fibers) is composed of protein. 2. Contrary to common speculation the central element is not the pairing surface of homologous chromosomes. 3. The L-C fibers, averaging 75–100 Å in width, extend from the lateral elements and meet to form the central element which is usually composed of four fibers. 4. During leptotene, homologous axial elements, although unpaired for most of their length, attach next to each other at the nuclear membrane. 5. Short segments of the chromatin fibers attach to the lateral elements. These points of attachment are clustered, producing the chromomeres seen by light microscopy. 6. The chromatin fibers extend out from the lateral element as loops. Lampbrush chromosomes are thus not restricted to oogenesis but are common to all meiotic chromosomes.Since the morphological features of the central element of the synaptonemal complex persist despite extensive deoxyribonuclease digestion, pairing is perhaps best visualized as a two-step process consisting of a) chromosomal pairing during which the proteinaceous synaptonemal complex pulls homologous chromosomes into approximate association with each other, and b) molecular pairing, which probably takes place in the area around the synaptonemal complex.Supported by NIH Grants GM-15886 and C-2568, and The Charles and Henrietta Detoy Research Fellowship.     

Identification of a structural protein component of rat synaptonemal complexes

Synaptonemal complexes (SCs) are evolutionarily conserved nuclear structures of meiotic cells which form during the zygotene stage of the first meiotic prophase and are responsible for the pairing of homologous chromosomes. Their formation appears to be a prerequisite for crossing-over events and proper chromosome segregation during the first meiotic division. Despite knowledge of their central role in genetic recombination processes very little is known about the molecular composition and the mechanisms governing the assembly of the SCs. In the present study we report on the characterization of a monoclonal antibody (SC14f10) which enabled us to identify a novel SC protein termed SC48. Protein SC48 has a Mr of 48,000 and migrates in two-dimensional gels with a pH value of 6.9. By means of immunogold EM we localized this protein to the central region of the SC. In cell fractionation experiments we recovered protein SC48 together with SC-residual structures in a karyoskeletal fraction of pachytene spermatocytes. Our results indicate that SC48 is a meiosis-specific structural protein component of the SC probably involved in the pairing of homologous chromosomes.     

Synaptonemal complexes with associated chromatin in a moth,Ephestia kuehniella Z.

Chromosome structure and pairing behaviour of the pachytene bivalents in the wildtype and in W chromosome mutants were studied using a microcentrifugation technique. The spread bivalents display a characteristic lampbrush structure with lateral loops having the typical appearance of nucleosomal fibers, in autosomes as well as in the W and Z chromosomes. While the autosomal loops are always completely dispersed by the spreading forces, the loops of the heterochromatic W chromosome frequently are found to be condensed in tangles. These tangles contain supranucleosomal globular particles of a diameter of 37.7±1.2 nm. — Pairing of the WZ can be complete or partial, probably depending on the stage of the pachytene. Incomplete pairing normally is interpreted as demonstrating non-homology. Pairing was weak, however, even between homologous segments of the W chromosome, which were introduced into the genome in homozygous form by a translocation chromosome.     

Meiotic prophase in anthers of asynaptic wheat

The light microscope showed that zygotene and pachytene were completely suppressed in pollen mother cells of an asynaptic mutant of Triticum durum; the chromosomes passed through a normal chromomeral leptotene condition and remained unpaired throughout prophase. The electron microscope confirmed the absence of synaptinemal complexes, as would be expected with no pairing. Prominent opaque axial cores were present in the chromatin from the onset of leptotene up to an indeterminate stage during prophase condensation. At an early time during condensation 150 Å particles appeared between chromatin masses. Coincident to the disappearance of axial cores from the chromatin, polycomplexes consisting of linearly associated core fragments arrayed in single layer sheets appeared between chromatin masses. The aligned fragments were invariably spaced about 625 Å from centre to centre; this is approximately half the distance between centres of the lateral elements (axial cores) of the synaptinemal complex of pachytene of synaptic sister seedlings. There was no central element between the associated fragments. The significance of these observations is discussed, as is also the essential difference between asynapsis and desynapsia.     

CRA-1 uncovers a double-strand break-dependent pathway promoting the assembly of central region proteins on chromosome axes during C. elegans meiosis

The synaptonemal complex (SC), a tripartite proteinaceous structure that forms between homologous chromosomes during meiosis, is crucial for faithful chromosome segregation. Here we identify CRA-1, a novel and conserved protein that is required for the assembly of the central region of the SC during C. elegans meiosis. In the absence of CRA-1, central region components fail to extensively localize onto chromosomes at early prophase and instead mostly surround the chromatin at this stage. Later in prophase, central region proteins polymerize along chromosome axes, but for the most part fail to connect the axes of paired homologous chromosomes. This defect results in an inability to stabilize homologous pairing interactions, altered double-strand break (DSB) repair progression, and a lack of chiasmata. Surprisingly, DSB formation and repair are required to promote the polymerization of the central region components along meiotic chromosome axes in cra-1 mutants. In the absence of both CRA-1 and any one of the C. elegans homologs of SPO11, MRE11, RAD51, or MSH5, the polymerization observed along chromosome axes is perturbed, resulting in the formation of aggregates of the SC central region proteins. While radiation-induced DSBs rescue this polymerization in cra-1; spo-11 mutants, they fail to do so in cra-1; mre-11, cra-1; rad-51, and cra-1; msh-5 mutants. Taken together, our studies place CRA-1 as a key component in promoting the assembly of a tripartite SC structure. Moreover, they reveal a scenario in which DSB formation and repair can drive the polymerization of SC components along chromosome axes in C. elegans.     

Mitotic and meiotic behavior of the chromosomes of the octet strain of Chlamydomonas reinhardtii

The normal vegetative culture chromosome number of the octet strain of C. reinhardtii was found to be 8. The difficulty of reconciliation of this number with the current genetic map of 16 linkage groups and the conceivability of revision of the map are discussed.Under some cultural conditions unstable vegetative apparent diploids are produced which tend to revert to haploids. It is suggested that in these cases cryptic connections of unknown nature may be retained between endoreduplicated sister elements and that these function for pairing in preparation for reversion to haploidy. Apparently intimate homologous chromosome pairing was found in normal zygotes no older than two or three hours, with light microscope examination. Electron microscope examination revealed paired chromatin elements separated by about 1000 Å at this stage. These may contain rudimentary synaptonemal complexes; none of the usual central region components or lateral elements were evident. Homologous chromosome pairing at this stage is of special interest because the major chromosomal meiotic DNA replication has been reported to occur at a much later stage of development; it has been previously postulated that crossing over precedes this replication, with the four elements necessary for crossing over at the 4-strand stage already present, due to the existence of some form of regular chromatid binemy (or its conceptual equivalent). Observations reported here are consistent with these interpretations.Conceivable relationships of these findings to problems of chromosome behavior in other eukaryotes are discussed.This work was supported by Grant GM 19582 and Research Career Development Award 5-KO3 GM 25988 from the U. S. National Institutes of Health.     

SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans

Synaptonemal complex (SC) formation must be regulated to occur only between aligned pairs of homologous chromosomes, ultimately ensuring proper chromosome segregation in meiosis. Here we identify SYP-3, a coiled-coil protein that is required for assembly of the central region of the SC and for restricting its loading to occur only in an appropriate context, forming structures that bridge the axes of paired meiotic chromosomes in Caenorhabditis elegans. We find that inappropriate loading of central region proteins interferes with homolog pairing, likely by triggering a premature change in chromosome configuration during early prophase that terminates the search for homologs. As a result, syp-3 mutants lack chiasmata and exhibit increased chromosome mis-segregation. Altogether, our studies lead us to propose that SYP-3 regulates synapsis along chromosomes, contributing to meiotic progression in early prophase.