SYNAPTONEMAL COMPLEXES IN RED ALGAE1,2

The presence of synaptonemal complexes in the nuclei of young tetraspore mother cells is described for the first time in the red algae. Synaptonemal complexes were found in Janczewskia gardneri Setchell, Levringiella gardneri Setchell, Gonimophyllum skottsbergii Setchell, and Polycoryne gardneri Setchell. The synaptonemal complexes consist of 2 lateral, dark-staining elements from which small fibrils extend to form a less densely staining central element. With minor variations, the dimensions and structure of these synaptonemal complexes correspond to those found in other organisms.     

Genetic Control of Meiosis in Rice, ORYZA SATIVA L. III. Effect of DS Genes on Genetic Recombination

The recombination frequency as influenced by five independent recessive ds genes was measured on three segments of different chromosomes of rice, Oryza sativa L. Each ds gene in the homozygous condition resulted in an almost equally reduced recombination frequency in the three segments. When the mean reduction in recombination frequency was related to the reduction of chiasma frequency, the five ds genes were divided into two types: in one type the reduction of chiasma frequency almost corresponded to the mean reduction of recombination frequency, and in the other the chiasma frequency was greatly reduced in comparison with the mean reduction of recombination frequency. Three of the five ds genes were found to belong to the former group. In both types, normal synaptonemal complexes were observed in pachytene cells homozygous for ds genes. This finding suggests that ds genes do not affect the formation of synaptonemal complexes which are regarded as the prerequisite structure for crossing over.     

Meiotic Structures in the Animal-Parasitic Nematode Ascaris megalocephala: Synaptonemal Complexes,Recombination Nodules,and Centrioles

Two synaptonemal complexes (SCs) were present in the pachytene nuclei of Ascaris megalocephala. The SC was tripartite and comprised of two lateral elements (25 nm) with a striated central element (25 nm) and a central region of 65 nm. Spherical recombination nodules were observed to be associated only with the central element, although they are non-existent in the related A. lumbricoides var. suum (Goldstein, 1977). The SCs were attached to the nuclear envelope at only one end, while the other end was free in the nucleoplasm. This lack of bouquet formation of the chromosomes is consistent with all other nematodes studied. Morphologically distinct sex chromosomes were not observed, which differs from the presence of five Y-chromosomes present in A. lumbricoides var. suum (Goldstein and Moens, 1976). Centrioles (0.2 µm wide) reproduced by budding off the parental centriole. The centrioles consisted of nine singlet microtubules connected by an electron-dense proteinaceous ring. This structure is consistent with centrioles described in other nematodes, yet distinctly different from the centriole structure observed in most organisms in which it consists of nine triplet microtubules without any connecting ring. Multiple synaptonemal complexes, or polycomplexes, are found in A. megalocephala and A. lumbriocoides var. suum. They appear as stacked SC and are present inside the nucleus during zygotene and in the cytoplasm at pachytene.     

Meiotic chromosome pairing and synaptonemal complex transformation in Culex pipiens oocytes

The synaptonemal complexes of the oocytes of the mosquito Culex pipiens quinquefasciatus have been reconstructed from serial sections. A diffuse structure, probably a chromocenter composed of centromeric heterochromatin, was present during pachytene. As no synaptonemal complexes were visible inside the chromocenter the continuity of the 2 arms of a bivalent was lost. The telomeric ends were clustered in a small area of the nuclear membrane in a bouquet arrangement; they were associated in pairs, and sometimes joined through a special structure. One pair was composed of the 2 telomeres of the shortest bivalent and a ring configuration was thus formed. The other 2 chromosomes may form one or two rings. During a short transitional stage, after the disappearence of the synaptonemal complexes, several thousand annuli, 1200–1500 A in diameter, were present in the nuclei. The annuli disappeared as material originating mainly from the transverse filaments of the synaptonemal complexes formed a capsule around the chromosomes during diplotene.     

Three-Dimensional Ultrastructural Karyotype Analysis from the Meiotic Parthenogenetic Nematode Heterodera betulae

Meiotic chromosome structure and function are described in the plant-parasitic nematode Heterodera betulae. Twelve synaptonemal complexes (SCs) were reconstructed from pachytene nuclei; therefore, n=12 is predicted for this species. Morphologically distinct sex chromosomes were not observed. Only one end of the SC is attached to the nuclear envelope, and there is no bouquet arrangement at pachytene. The structure of the SC in this meiotic parthenogenetic nematode was different than in other nematodes that reproduce via amphimixis; a striated central element with transverse filaments was not observed. Multiple SCs, or polycomplexes, were present in the nucleus. Recombination nodules were not observed. The centrioles were comprised of nine doublet microtubules connected by a ring, which is a distinct modification from the typical nine triplet microtubules without any interconnecting structure.     

Solving a meiotic LEGO puzzle: transverse filaments and the assembly of the synaptonemal complex in Caenorhabditis elegans

The structure of the meiosis-specific synaptonemal complex, which is perhaps the central visible characteristic of meiotic prophase, has been a matter of intense interest for decades. Although a general picture of the interactions between the transverse filament proteins that create this structure has emerged from studies in a variety of organisms, a recent analysis of synaptonemal complex structure in Caenorhabditis elegans by Schild-Prüfert et al. (2011) has provided the clearest picture of the structure of the architecture of a synaptonemal complex to date. Although the transverse filaments of the worm synaptonemal complex are assembled differently then those observed in yeast, mammalian, and Drosophila synaptonemal complexes, a comparison of the four assemblies shows that achieving the overall basic structure of the synaptonemal complex is far more crucial than conserving the structures of the individual transverse filaments.     

SC-karyotyping on electronic microscopy (EM) analysis of synaptonemal complexes (SC) spermocytes of silver fox (Vulpes fulvus)

We present an electronic microscopy (EM) analysis of synaptonemal complexes (SC) spermatocytes of male silver fox Vulpes fulvus at the pachytene stage. The SC-karyotypes of pachetene cells were made and described. Knowledge of normal SC-karyotype is necessary to reveal synaptic abnormalities of autosome and sex bivalents during the pachytene. It was indicated that EM analysis of SC-spermatocytes—the study of synaptonemal complexes in agricultural animals—is a very good instrument for comparative analysis of normal SC-karyotype of foxes that carry chromosomal abnormalities and in fur-bearing animals as well.     

Spermatogenesis in Bombyx mori. II. The ultrastructure of synapsed bivalents

In Bombyx mori the male is the homogametic sex, crossing over occurs only in males, and chiasmata are observed in spermatocytes, but not in oocyte nuclei. If the assembly of synaptonemal complexes is an essential prerequisite for genetic crossing over and chiasmata formation, then the nuclei of Bombyx spermatocytes should contain synaptonemal complexes. Synaptonemal complexes were found in spermatocytes from young four instar larvae. The structure of meiotic bivalents is described using micrographs taken with 100 and 1000 KV electron microscopes. These data together with that from the literature are used to construct a three-dimensional model of the synaptonemal complex and to suggest its method of origin and its function during crossing over.     

Alteration of meiotic chromosomal pairing and synaptonemal complexes by cycloheximide

When cells are exposed to cycloheximide during the synaptic period of meiotic prophase, the structure of the synaptonemal complex is markedly altered. The bulk of the lateral component is removed. When lily zygotene microsporocytes are subsequently transferred into a culture medium free from cycloheximide, normal synaptonemal complexes are again seen. Modification of the structure of the synaptonemal complex by treatment with cycloheximide for 4 days has little permanent effect on meiosis except at late zygonema or early pachynema. Treatment at this time produces meiocytes in which no synaptonemal complexes reform. When these cells proceed into diplotene and diakinesis they are devoid of chiasmatic chromosomes. The data suggest that the synaptonemal complex is essential if chiasmata are to be formed, and that a unique period exists when the formation can be interrupted.This work was supported by grants from the National Science Foundation (GB 5173X and GB 6476) and the National Institutes of Health (GM 16882).     

Meiotic recombination and synaptonemal complexes in Saccharomyces cerevisiae.

Summary The course of meiotic recombination, gene conversion and crossing-over, was investigated in Saccharomyces cerevisiae. Gene conversion was used as the selected event by removing cells from a medium inducing and promoting meiosis to a vegetative growth medium selective for convertants. Gene conversion started to increase at the same time as DNA synthesis, and nuclei entered a phase where the chromatin appeared as thread-like structures. Crossing-over of linked and unlinked markers also started early but remained at a low level until synaptonemal complexes were formed. However, gene conversion and a limited amount of crossing-over could be completed without synaptonemal complexes. It was concluded that meiotic recombination in yeast can occur as early as during DNA synthesis and does not require the function of synaptonemal complexes. Moreover, the low incidence of crossing-over early in meiosis is attributed to a low frequency of strand isomerization.     

Dependence on genic balance for synaptonemal complex formation in Drosophila melanogaster

Electron microscopic examination of gonads of Drosophila melanogaster with different genotypes, including a metafemale 3X;2A and an intersex XXY;3A have revealed that the formation of synaptonemal complexes is controlled by the genic balance, i.e., the ratio of X chromosomes to autosomes. The Y chromosome is not involved in the genetic control of the formation of precursors of the central element of synaptonemal complexes in males, nor does it disturb their formation in XXY females. Hyperploidy for sections 1-3A and 18A-20 of the X chromosome does not lead to the appearance of synaptonemal complexes in males and does not interfere with their formation in females. Females hyperploid for extensive regions of the X chromosome (sections 1-11A, 11A-20, and 8C-20) are fertile and show apparently normal formation of synaptonemal complexes. Hyperploidy for sections 8C-11A of the X results in a sharp decrease in the viability of females, in abnormal differentiation of ovary cells, and in the lack of synaptonemal complexes. These data suggest a possible important role for the sections 8C-11A in the genic balance controlling the formation of synaptonemal complexes in D. melanogaster. The lack of synaptonemal complexes in hypoploid females may be the result of abnormal cell differentiation in gonads.     

Abnormal meiosis in bisporic strains of white button mushroom Agaricus bisporus (Lange) imbach

A formerly developed method of microspreading of mushroom basidial nuclei was applied to study meiotic prophase I in bisporic white button mushroom (Agaricus bisporus) strains. Meiotic recombination and assemblage of axial structures (axial elements and synaptonemal complexes) of chromosomes in meiotic prophase I are interrelated. It is known that the frequency of meiotic recombination is reduced in the bisporic A. bisporus variety. We showed that formation of axial structures of meiotic chromosomes in bisporic strains of this mushroom was disrupted. The anomalous phenotypes in spread prophase nuclei are diverse. In leptotene and early zygotene, many nuclei contain abnormal, often short, and, as a rule, few chromosomal axial elements. The abnormalities in the formation of synaptonemal complexes at the zygotene-diplotene stage are of the same kind and even more pronounced. We discovered an important feature of meiosis in A. bisporus associated with fruit-body morphogenesis. Meiosis starting in basidia (meiocytes) of young closed fruit bodies is accompanied by disruption of chromatin condensation in prophase I and, probably, is arrested. After partial veil breakage, the course of meiosis normalizes. Preparations with clearly observable chromosomal axial structures can be obtained only at this stage of fruit-body development.     

Sequential study of the synaptonemal complex in Syrian hamster (Mesocricetus auratus) and mouse (Mus musculus) oocytes by light and electron microscopy

We describe the behaviour of synaptonemal complexes (SCs) in Syrian hamster and mouse oocytes. InMesocricetus auratus, synaptonemal complexes can be observed from birth up to 7 days of life. In foetuses fromMus musculus, synaptonemal complexes can be observed from the 14th day of gestation up to the first day post-partum, when the cells enter the dictyotene stage. In both species, synaptonemal complexes show, in general, the same morphology described in male cells by light and electron microscopy, with the exception that the axes of the sex bivalent are not identifiable. The leptotene stage can be identified although it is probably of short duration. Only one type of zygotene (zygote ne II of Dietrich and Mulder(Chromosoma 88: 377), 1983) has been observed. In the hamster we also describe a desynaptic diplotene stage previous to the desintegration of the SCs. In oocytes from both species late pairing (or precocious separation) of a single bivalent can be seen in a few cells. Interlocking of some bivalents with delayed pairing of the affected region is rather frequent. Furthermore, hamster oocytes may show heterosynapsis of the telomeres of autosomal bivalents by pachytene.     

The pachytene synaptonemal complex complement of the cat

Surface spreads of pachytene spermatocyte nuclei from two cats were used to construct a synaptonemal complex karyotype for the cat. It was possible to recognise the 18 autosomal synaptonemal complexes by reference to a published light microscopic banded somatic karyotype. Some variation from the somatic karyotype was noted, presumably as a result of differential contraction during prophase I. The X and Y chromosome axes were joined by a synaptonemal complex in many of the nuclei, but the structure of the unpaired portion of the X axis was quite variable. In some nuclei it was highly contracted, while in others it was extended and often was split into two or more axes. In most nuclei the autosomal synaptonemal complexes had numerous axial twists.     

Synaptonemal complexes in antheridia of Achlya ambisexualis E87

This is the first report of longitudinal sections of synaptonemal complexes in oömycetous fungi. These indicators of meiosis were observed in antheridial nuclei of Achlya ambisexualis E87. They were attached to a platelike structure at the inner membrane of the nuclear envelope. The lateral elements were separated from each other by an average distance of 160 nm. These results provide new ultrastructural evidence for gametangial meiosis in Oömycetes.     

Damage to synaptonemal complex structure and peculiarities of selection of mouse spermatocytes I at response to drug administration

Using immunocytochemistry methods, the structure of synaptonemal complexes (SC) of chromosomes in spread nuclei of primary spermatocytes of mice at 1, 10, and 36 days after the 10-day intraperitoneal administration of antibacterial preparations of three pharmacological groups: furacilin, an antiseptic derivative of nitrofuran; cifran, an antibiotic from the group of fluoroquinolones; and sextaphage, a polyvalent piobacteriophage was investigated. The maximal number of damages in the structure and behavior of synaptonemal complex was revealed on the first day after the end of preparation administration. On days 10 and 36, the total number of damages in SC structure decreased gradually. On the first day after the end of the administration of cifran and sextaphage in 41.8 and 25% of nuclei, respectively, the fragmentation of synaptonemal complexes was revealed and, in males to whom furacilin had been administered, the fragmentation of synaptonemal complexes was identified in 100% of nuclei. Multiple chromosome fragmentation is a meiotic catastrophe and results in the degeneration of cells without enabling the mechanism of pachytene arrest. The features of pachytene arrest were revealed in the nuclei of primary spermatocytes with the violation of chromosomes pairing. After the administration of sextaphage, circle structures released from the lateral elements of SC and are dyed with antibodies to SCP3 protein.     

The synaptonemal complex as part of the nuclear matrix of the flour moth, Ephestia kuehniella

A nuclear matrix fraction was prepared from ovaries of the achiasmatic flour moth, Ephestia kuehniella, by removal of the chromatin, using detergent treatment of homogenized ovaries or dissected ovary tips followed by DNase digestion and high salt extraction. Removal of DNA and histones from the nuclei was demonstrated by Feulgen staining and polyacrylamide gel electrophoresis (PAGE), respectively. By light microscopy, ribbon-like structures similar in dimension to the synaptonemal complex were observed in the oocyte after digestion of the chromosomes. Electron microscopic examination of matrix preparations of pachytene cells showed a defined synaptonemal complex structure with both lateral and central elements. Such structures were not found in either the fully differentiated nurse cells or in follicle cells which were exposed to the same preparative technique concurrently. However, in early post-pachytene nurse cells the typical polycomplex structures, formed in these cells from the synaptonemal complex, were found in nuclear matrix preparations. The results suggest an association of synaptonemal complexes with the nuclear matrix.     

Synaptonemal complex proteins

Synaptonemal complexes were isolated from rate spermatocytes for the purpose of biochemical and morphological analysis. Several monoclonal antibodies were elicited against purified synaptonemal complexes to study the composition and assembly of these structures. Four classes of antibodies could be discriminated according to the polypeptides that they recognize on Western blots of purified synaptonemal complexes, namely antibodies recognizing (i) a 190-kDa polypeptide; (ii) a 30- and a 33-kDa polypeptide; (iii) two polypeptides with molecular weights of about 120 kDa; and (iv) polypeptides with molecular weights of 66-55 kDa. The localization of these antigens within spermatocytes was analyzed light microscopically, by means of the immunoperoxidase technique and ultrastructurally, by immunogold labelling of surface-spread spermatocytes. The 66- to 55-kDa polypeptides are not confined to synaptonemal complexes; rather, these polypeptides appear to be chromosomal components. The 190-, 30-, and 33-kDa polypeptides make part of the lateral elements of paired as well as unpaired segments of synaptonemal complexes. The 120-kDa polypeptides were localized on the inner edge of the lateral elements, specifically in paired segments of synaptonemal complexes. The distribution of the 190-, 120-, 30-, and 33-kDa polypeptides within the testis was analyzed by immunofluorescence staining of cryostat sections. All these polypeptides turned out to be specific for nuclei of zygotene up to and including diplotene spermatocytes. Only in some early spermatids could the 190-, 30-, and 33-kDa polypeptides be detected, presumably in remnants of synaptonemal complexes.(ABSTRACT TRUNCATED AT 250 WORDS)     

Mutation of the Mouse Syce1 Gene Disrupts Synapsis and Suggests a Link between Synaptonemal Complex Structural Components and DNA Repair

In mammals, the synaptonemal complex is a structure required to complete crossover recombination. Although suggested by cytological work, in vivo links between the structural proteins of the synaptonemal complex and the proteins of the recombination process have not previously been made. The central element of the synaptonemal complex is traversed by DNA at sites of recombination and presents a logical place to look for interactions between these components. There are four known central element proteins, three of which have previously been mutated. Here, we complete the set by creating a null mutation in the Syce1 gene in mouse. The resulting disruption of synapsis in these animals has allowed us to demonstrate a biochemical interaction between the structural protein SYCE2 and the repair protein RAD51. In normal meiosis, this interaction may be responsible for promoting homologous synapsis from sites of recombination.