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Meiosis in Mesostoma Ehrenbergii Ehrenbergii. IV. Recombination

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Meiosis in Mesostoma Ehrenbergii Ehrenbergii. IV. Recombination Copyright 0 1989 by the Genetics Society of America Meiosis in Mesostoma ehrenbergii ehrenbergii.IV. Recombination Nodules in Spermatocytes and a Test of the Correspondenceof Late Recombination Nodules and Chiasmata Joy A. Croft and Gareth H. Jones Department of Genetics, University of Birmingham, Birmingham B15 ZTT, England Manuscript received July 7, 1988 Accepted for publication October 13, 1988 ABSTRACT Male meiosis in Mesostoma ehrenbergii ehrenbergii (2x = 10) is characterized by extreme restriction of chiasma formation; 3 pairs of chromosomes form bivalents at metaphase 1 which are associated by single very distally localized chiasma, while twopairs of chromosomes remain as unpaired univalents. Electron microscopical three-dimensional reconstruction analysis of serial sections hasbeen applied to 20 pachytene spermatocyte nuclei. In each nucleus three short stretches of synaptonemal complex (SC) were found, confined to a localized branched lobe of the nucleus, confirming the findings of an earlier study. The majority of reconstructed nuclei show that each of the three SC segments has a single prominent recombination nodule ("late" RN) associatedwith it. Late RNsin this system therefore show an excellent correspondence with metaphase I chiasmata, in contrast to a previous report. M. e. ehrenbergii is therefore not an exception to thehypothesis that meiotic exchange requires a functional late RN. A few nuclei had two, one or no RNs; these presumably represent nuclei that are not at thestage of maximum RN presence. Although M. e. ehrenbergii shows pronounced chiasma localization at the light microscope level, at the ultrastructural level RNs are widely distributed along the 5-10 pm of SC formed in each bivalent, indicating that genetic exchanges are not restricted to particular localized sitesbut occur at a large number of DNA sequences. HE curious meiotic systems found in the oocytes respond to the threechiasmatically associated bivalent T and spermatocytes of the Rhabdocoel planarian ends in spermatocyte first metaphases. worm Mesostoma ehrenbergii ehrenbergii(2x = 10) have This unusual andinteresting system presents an a long history of investigation (SCHNEIDER1883; VON excellentopportunity to test the proposedcorre- Voss 1914; VALKANOV1938; HUSTEDand RUEBUSH spondence between recombination nodules and clas- 1940; KEYL and GOLTENBOTH1972; GOLTENBOTH sical chiasmata. Recombinationnodules (RNs) are 1973) and were recently the subject of detailed rein- dense spherical or ellipsoid structures, about 100 nm vestigation by light and electron microscopy (OAKLEY in diameter, which occur in close association with the and JONES1982; OAKLEY1982, 1985). These studies central elements of SCs in a wide range of eukaryotes confirmed previous observations that spermatocytes (reviewed by VON WETTSTEIN,RASMUSSEN and HOLM consistently form only three bivalents at metaphase I, 1984). Their role as structuresmediating meiotic each associated by a single very distal chiasma (OAK- recombination was firstproposed by CARPENTER LEY and JONES 1982). The remaining four chromo- (1975) and has received considerable support from somes are present as univalents which nevertheless other investigations across a wide range of organisms regularly achieve accurate segregation at anaphase I (reviewed by CARPENTER1979b; VON WETTSTEIN, (OAKLEY1985). A parallel study of oocyte meiosis RASMUSSENand HOLM1984). More recently it has revealed that all five chromosome pairs exhibitachias- been proposedthat two types of RNs exist which differ matic association fromdiplotene through to meta- in their chronology of appearance (early vs. late), in phase I (OAKLEY1982). their frequencies and distributions, and generally if An earlier ultrastructural investigation of mid-pro- not alwaysin theirmorphologies (RASMUSSENand phase Ispermatocytes, involving three-dimensional HOLM1978; CARPENTER1979b). Early RNs are con- reconstruction of six nuclei, showed that synaptone- fined to zygotene in some species, but are retained mal complex (SC) formation and hence chromosome into early pachytene in others. They have been sug- pairing is restricted to three shortstretches occupying gested to have a role in promoting homologous pair- a lobed region of the nucleus (OAKLEYand JON= ing during zygotene (ALBINIand JONES1987; CAR- 1982). In other words, chromosome pairing in sper- PENTER 1987) and they may also mediate gene con- matocytes of this species is constitutively incomplete. version at thattime (RASMUSSENand HOLM 1978; It is deduced that pairing is limited to the ends of CARPENTER1979a, 1987). Late RNs are restricted to three chromosome pairs which are presumed to cor- pachytene and they are hypothesized to be involved Genetics 141: 255-262 (February, 1989) 256 J. 256 andA. Croft G. H. Jones in some or all aspects of crossing over(reciprocal microscope and selected nuclei were photographed at mag- recombination, exchange) during pachytene. Thishy- nifications of 6,000-7,500. SCs and RNs were traced from enlarged photographic prints onto acetate sheets and SC pothesis is based on the close correspondences which lengths and RN positions were measured using a Summa- havebeen observed between thenumbers and/or graphics digitizer linked to a BBC microcomputer which distributions of late RNs and crossovers or cytological was programmed toallow for section thickness in calculating chiasmata in a wide variety of species (CARPENTER true SC lengths and RN positions. 1979b; VON WETTSTEIN,RASMUSSEN and HOLM 1984).However, deficiencies of lateRN numbers RESULTS comparedto chiasmata/crossovers havebeen re- ported in many species (ALBINIandJoNEs 1988), from Testis organization: M. e. ehrenbergzi has a pair of which it is inferred that late RNs are ephemeral struc- long lobulated testes which lie along each side of the tures in these species; that is they are present only pharynxand vitelline glands. Inadult animals the transiently during pachytene and consequently the full testes occupy about half the body length andmake up complement of late RNs may not be present simulta- roughly 25% of body volume. There is no obvious neously. sequential arrangement of spermatogenic stages in the Applied to M. e. ehrenbergzi male meiosis, the late testis. Although cells at the same stage of spermato- RN hypothesis predicts that each of the three short genic development are grouped together in synchro- SC stretches should contain a single late RN at some nized clusters, groups of cells at different stages bear time during theprogression of the cell through pach- no apparentrelation to each other and occur scattered ytene, since each of the bivalents has one chiasma at throughout the testis in an apparently unordered ar- metaphase 1. Because of the relatively short lengths rangement (OAKLEYand JONES 1982). Spermatogenic of these SCs, this prediction should be relatively easy cells containing SC are morphologically distinct from to test. Althoughsix nuclei were thoroughly examined other cell types in terms of nuclear shape and chro- in the earlierstudy by OAKLEYand JONES (1982), RNs matin condensation as well as their possession of SC. were not seen. Since this, if confirmed, would at least These so-called "SC cells" are regarded asa develop- provide an exception to the so-far universal observa- mental substage of a single population of spermato- tion that a meiotic exchange requires a functional late genic prophaseI cells. They contain roughly spherical RN, a further careful search for RNs was considered or ellipsoidal nuclei but with a characteristicbranched worthwhile. lobearising from a localized part of eachnucleus (Figure 1). The main body of each nucleus is 14-16 MATERIALSAND METHODS pm in diameter, and the lobe projects 6-8 pm from the main nucleus. Culture conditions: Laboratory cultures of M. e. ehren- Synaptonemal complexes: Twenty nuclei contain- bergii were raised from dormantwinter eggswhich had been ing SC werereconstructed from serial sections. In cold-treated (4" for at least 12 weeks) to overcome their natural diapause. Young animals were kept in filtered pond every case the SCs are confined to the projectinglobed water and fed on brine shrimps which had been washed to region and the main body of each nucleus is entirely remove all traces of brine. The animals were used when devoid of SC except for a limited zone at the base of about 4 weeks old. the lobe. The morphology of the SC is somewhat EM preparation: Whole animals were fixedin 4% glutar- atypical in this species. Its most striking feature is the aldehyde in phosphate buffer (pH 7.2) for 4 hr at room temperature. The material was post-fixed in 2% osmium prominent pale central region containingvery a dense tetroxide in phosphate buffer (pH 7.2) for 2 hr and then central element (Figure2). The lateral elementsflank- dehydrated through an alcohol series. Some animals were ing the central region areindistinct and their density stained with phosphotungstic acid (PTA), in which case the closely matches that of the adjoining chromatin. osmium tetroxide step was omitted and entireanimals were Each reconstructed nucleus was found to contain treated with 1% alcoholic PTA at 20" for 10-1 6 hr after the alcohol dehydration series and before embedding. En- just three short SC stretches, as previously described tire animals were embedded in Epon 8 12 which was polym- by OAKLEYand JONES (1 982).Each SC occupies one erized at 60" for 20 hr. Section series were cut from four branch of the lobed region and terminates distally different animals (see
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