Chromosoma (Bed) (1986) 94: 94-102 CHROMOSOMA �9 Springer-Verlag 1986

Synaptonemal complexes and chromosome chains in the rodent Ellobius talpinus heterozygous for ten Robertsonian translocations Yu.F. Bogdanov 1, O.L. Kolomiets 1, E.A. Lyapunova 2, I.Yu. Yanina z, and T.F. Mazurova ~

N,I. Vavilov Institute of General Genetics of the USSR Academy of Sciences, B-333 Moscow, I 17809, USSR 2 N.K. Koltzoff Institute of Developmental Biology of the USSR Academy of Sciences, Moscow, 117334, USSR

Abstract. Synaptonemal complexes (SC) in four Ellobius talpinus males heterozygous for ten Robertsonian transloca- tions were examined with an electron microscope using a surface-spreading technique. A total of 136 late zygotene and pachytene spermatocytes were examined. From one to three completely paired SC trivalents were found in each early pachytene spermatocyte. The lateral elements of the short arms of the acrocentric chromosomes in these triva- lents were joined with an SC thus forming the third arm of the SC trivalent. At the same stage a few SC trivalents did not contain lateral elements in the pericentromeric re- gion of the metacentric chromosomes and remained un- paired in this region up to mid pachytene. At zygotene and pachytene from two to eight SC trivalents were joined into chains due to formation of SCs between the short arms of acrocentrics of other SC trivalents. These chains are fre- quent at late zygotene, but are resolved during pachytene into individual trivalents. It is proposed that pairing and SC formation between the short arms of the acrocentric chromosomes results from the monosomy of the short arms and partial DNA homology between these heterochromatic regions. Since crossing over probably does not take place in these segments, the chromosomal chains may subse- quently be corrected into trivalents by a dissolution of the SCs combining adjacent trivalents. The correction and dis- joining of chains may not be effective in all cells. The cells in which the chains are retained are assumed to be arrested at the pachytene stage.

Introduction

Robertsonian (Rb) translocations are known to play an essential role in the evolution of plant and animal karyo- types (Navashin 1926, 1932; Mattey 1970; White 1973). The nature of Rb translocations has been elucidated in the work of Moses et al. (1979) who studied surface-spread syn- aptonemal complexes (SCs) in pachytene spermatocytes of lemurs heterozygous for Rb translocations. It was shown that Rb metacentrics paired with homologous acrocentrics forming a trivalent. The Rb metacentric contained only one kinetochore and the total length of the SC lateral elements belonging to the two acrocentrics exceeded that of the meta- centric. Thus, it is apparent (Moses et al. 1979) that in this case the formation of Rb metacentrics is a result of a true

reciprocal chromosome translocation based on the break- reunion mechanism and is accompanied by the loss of part of the chromosome material including one centromere as predicted by Navashin (1932).

The study of SC trivalents in lemurs (Moses et al. 1979) and mice (Gropp and Winking 1981; Demin et al. 1984) demonstrated that in the centromeric region of a trivalent a gradual length adjustment of the lateral elements of the acrocentrics to the lateral element of the metacentric oc- curred. At the same time, there was nonhomologous synap- sis of the two short arms of the acrocentrics. Recently it has been demonstrated that synaptic adjustment, i.e. non- homologous pairing and length adjustment of heterologous lateral elements is a routine phenomenon in cases of hetero- zygosity for chromosome duplications, deletions, and inver- sions (see Moses and Poorman ~ 984).

The present study investigates SC formation and synap- tic adjustment in heterozygosity for multiple Rb transloca- tions. The rationale was that this material would be favour- able for studying different phases of SC trivalent formation. The rodent Ellobius talpinus Pall. was used the karyotype and biology of which are well known to one of the authors of this paper (E.A.L.). This superspecies is characterized by a wide karyotype variability associated with Rb translo- cations. There are several stable chromosomal forms in na- ture including forms having 2n = 34 and 2n= 54 (Lyapu- nova et al. 1974). These two forms have equal numbers of chromosome arms (NF = 56) but differ in the number of metacentrics and acrocentrics in their karyotypes: the "low-chromosomal" form (2n = 34) has ten pairs of Rb metacentrics, and both forms have one pair of identical metacentrics (Lyapunova and Vorontsov 1978). Under nat- ural and laboratory conditions these forms can mate and produce hybrid progeny (2n =44) which have low fertility but are nevertheless able to reproduce (Lyapunova 1983; Lyapunova and Yakimenko 1985). This ability determines the existence of a complete "Robertsonian fan" of chromo- some variability in natural populations of this animal in the Pamir-Altai region (Lyapunova et al. 1980, 1984; Vor- ontsov and Lyapunova 1984).

Materials and methods

Individuals of Ellobius talpinus caught in the Surkhob river valley (Tajik SSR) in 1983 were kept and reproduced in a vivarium. Meiosis was characterized in two males having

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Fig. 1. Surface-spread AgNO3-stained synaptonemal complexes (SCs) from a pachytene spermatocyte of Ellobius talpinus (2n = 54). No kinetochores are revealed; 27 SCs are visible. X Y sex bivalent. Bar represents 10 pm

2n= 34 and three males having 2n= 54 by the surface- spreading technique (Dresser and Moses 1980). F1 hybrids between forms with 2n = 34 and 2n = 54 in reciprocal crosses were obtained. In this work we studied meiosis in four F1 males from different parental pairs. In two animals one of the testes was used to prepare samples for electron mi- croscopy (see below) and the other was used for light mi- croscopy. In the remaining two animals both testes were used for electron microscopy. In all, 136 cells at the zygo- tene and pachytene stages were examined with an electron microscope.

Meiotic cells were prepared for electron microscopy by the method of Dresser and Moses (1979), examined with a light microscope and then photographed at a tow magnifi- cation in a JEM-100B electron microscope. The subdivision of the pachytene stage into early, mid, and late pachytene was based on the morphology of the sex bivalent (Moses 1981). The details are described in Results.

The karyotypes of somatic cells were studied in bone marrow cells as described previously (Lyapunova and Vor- ontsov 1978). Metaphase chromosomes were stained by the standard methods for G- and C-banding (Sebright 1971; Sumner 1972).

Results

Electron microscopic examination of SCs in spermatocytes of two males with 2n = 34 and three males with 2n= 54 revealed SCs that were typical of mammals and had no

numerical or structural anomalies (Fig. 1). The somatic kar- yotypes of animals with 2n = 34 and 2n = 54 are also known (Lyapunova and Vorontsov 1978; Lyapunova et al. 1980).

Analysis of bone marrow cell metaphases in F1 hybrids resulting from mating rodents with 54 and 34 chromosomes showed that all of them had 2n = 44, the number of chromo- some arms being 56. Accordingly, 12 metacentric and 32 acrocentric chromosomes were observed in the karyotypes of these hybrids. Only one pair of homologues was dis- covered among the metacentrics and 6 pairs, including a pair of sex chromosomes, were found among the acrocent- rics. The remaining 20 acrocentrics turned out to be homol- ogous to the arms of the 10 remaining metacentrics by G- banding (Fig. 2). This karyotype is the one expected for the hybrids.

In these hybrids the formation of seven bivalents and ten trivalents was expected in pachytene. The electron mi- croscopic study of pachytene spermatocytes confirmed this expectation with respect to the number of bivalents, while with respect to the number of trivalents the case was more intricate. At zygotene and pachytene three different pairing configurations were observed: (1) completely paired triva- lents, (2) incompletely paired trivalents, and (3) chains of partially paired metacentric and acrocentric chromosomes. The frequencies of these configurations changed from zygo- tene through the different substages of pachytene. The pa- chytene stage was subdivided into an early, a mid, and a late substage on the basis of morphological changes in the sex bivalent as outlined below.

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Fig. 2. G-banded karyotype of Ellobius talpinus F1 hybrids (2n=44) obtained by crossing two karyomorphs, 2n = 34 and 2n= 54. The karyotype consists of I pair of metacentrics, 6 pairs of acrocentrics, 10 Robertsonian metacentrics and 20 acrocentrics homologous to the arms of the Robertsonian metacentrics

Table 1. Mean number of synaptomal complex configurations in Ellobius talpinus heterozygous for ten Rb translocations (2n = 44)

Meiotic Number of Bivalents Trivalents Total number stage cells of bivalents +

studied Free Included Included Free Free Free trivalents closed in chains in chains broken open closed

Late zygotene 2 5.5 1.5" 7 0 1.5 1.5 7+ 10 Pachytene:

early 4 7 0 3.7 4 0.3 2 7 + 10 mid 7 6.9 0.t b 3.9 2 0.6 3.5 7 + 10 late 4 7 0 0 2 0 8 7 + 10

" Includes three cases of autosomal bivalents participating in chromosomal chains within two cells b Includes one case of a sex bivalent participating in a chain

Sex bivalent

Sex chromosomes in E. talpinus males are of equal size and have similar G-band ing pat terns (Lyapunova and Voront- soy 1978; Vorontsov et al. 1980). In surface spreads it is possible to identify a sex bivalent of spermatocytes from very late zygotene or early pachytene onwards.

In early pachytene one can see short SCs at both ends of a sex bivalent, the large middle segment of the lateral elements being unpaired. One of the lateral elements carries a dense nucleolar body (Fig. 3a). The unpaired parts of both lateral elements are of the same thickness, equal to the thickness of the lateral elements of autosomes. In some spermatocytes of F1 heterozygotes we observed asynapsis at one end of the sex bivalent (Fig. 8).

In mid pachytene (Fig. 3 b) the lateral elements of the sex bivalent are twice as long as in early pachytene. The nucleolar body has also grown. The lateral elements are a little thicker than at the previous substage. Their unpaired segments usually cross each other, forming a figure 8. One can see splitting and branching of the unpaired parts of the lateral elements (Fig. 3 b). The lateral components are surrounded by a cloud of electron-dense material .

In late pachytene (Fig. 3 c) the lateral elements are ex- tremely branched and have some gaps. They are approxi- mately five times longer than at early pachytene. A short

SC is present at one end of the bivalent. The electron-dense material sometime masks the lateral elements.

Autosomal bivalents

SC development in autosomes starts from one or both ends of the chromosomes. No init iat ion of synapsis was observed in the internal par ts of autosomes. Bivalents in which initia- t ion of synapsis has occurred at one end only are referred to as open bivalents, while a bivalent is said to have a closed configurat ion when synapsis starts from both ends. At the end of zygotene, pair ing of all six au tosomal biva- lents with an SC is complete except for a few spermatocytes. In these only four au tosomal bivalents were found at early pachytene. Two other bivalents were included in mult ichro- mosomal chains (Table 1).

Trivalents

Pairing of the lateral element of an R b metacentric chromo- some with two acrocentrics started at zygotene from the telomeres of the metacentric chromosome and proceded in the direction of the centromere region (Fig. 4a). The lateral element of the metacentric chromosome was often discon- t inuous in the centromeric region (Fig. 4c). All tr ivalents identifiable at early to mid zygotene stages were of the open type, i.e. with no pair ing between the short arms of the

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Fig. 3 ~-c. Synaptonemal complexes (SCs) of a sex bivalent of Ello- bius talpinus FI hybrid (2n =44). The lateral elements are of equal length but one of them carries a nucleolar body. Hollow arrowheads indicate the SCs at the telomere ends of the sex bivalent. A SC of an autosome; LE unpaired lateral element participating in a chain of autosomes (see Fig. 5); S split of the lateral element of the sex chromosome, a Early pachytene; b mid pachytene; c late pachytene; lateral elements are branched. Bars represent 1 ~tm

acrocent r ic c h r o m o s o m e s (Table 1). The dis tance be tween the shor t a rms o f the acrocent r ics pa r t i c ipa t ing in a t r iva lent was a few mic rome te r s (Fig. 4a).

As early as late zygotene one c losed t r iva lent in each spe rma tocy te can be seen, i.e. pa i r ing is comple te and the short a rms of the acrocent r ics pa r t i c ipa t ing in the t r iva lent are pa i red and fo rm a th i rd a rm o f the t r iva lent (Fig. 4 b). The a rm is s u r rounded by m o r e dark ly s ta ined c h r o m a t i n cons idered as he t e roch roma t in .

Fig. 4 a-d. AgNO3-stained synaptonemal complexes (SCs) of triva- lents at late zygotene-early pachytene from surface-spread sperma- tocytes of Ellobius talpinus F1 hybrids (2n=44) heterozygous for Robertsonian translocations. A 1, A'I the axial elements of the acro- centrics; M the axial element of the metacentric; solid arrowheads indicate SCs between short arms of acrocentrics; hollow arrowheads indicate gaps in the pericentromeric regions of the axial elements of the metacentrics, a An incompletely paired SC trivalent: only distal parts of the lateral elements are paired; b an example of a completely paired (closed) SC trivalent; c a broken SC trivalent; d an SC trivalent in which the formation of an SC segment between the short arms of the acrocentrics is completed while the axial element in the pericentromeric region of the metacentric is discon- tinuous. Bars represent i ~tm

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Fig. 5. Part of a surface-spread, late zygotene nucleus showing a chain of three incompletely paired trivalents, A1, A'~, MI the lateral elements of the first synaptonemal complex (SC) trivalent in the chain; A2, A'z, M2 and Aa, A'3, M3 the same for the second and the third trivalents, respectively. The solid arrowheads indicate SC segments between the short arms of the acrocentrics from adjacent trivalents. Bar represents 10 gm

Table 2. Synaptonemal complex configuration, interlocking and breaks in spermatocytes of Ellobius talpinus heterozygous for ten Rb translocations (2n =44)

Animal Cell Meiotic Inter- Breaks in Lateral elements Formulae of the chains No, No. stage lockings lateral joined

element into chains

15 16 Late zygotene 1 7 11 ; 6; 5 31i I + 111 ; 2ni ; 1 In + 111 18 17 Late zygotene 1 2 15 ; / I 5m; 3t1i+ 111

Mean 1 4.5 24

15 2 Early pachytene 0 5 9 3111 15 7 Early pachytene 0 9 6; 6 211t; 2111 15 10 Early pachytene 2 8 6; 6 2m ; 2111 15 11 Early pachytene 0 6 12 4tn

Mean 0.5 7 11.3

15 1 Mid pachytene 1 6 15 5m 15 3 Mid pachytene 0 1 12 4111 15 8 Mid pachytene 0 3 6 2111 15 14 Mid pachytene 1 5 15 5111 15 15 Mid pachytene 0 3 12; 6 4111 ; 21i 1 15 34 Mid pachytene 1 7 6; 5 2ii1; 11ii+ 111 18 17 Mid pachytene 1 3 6 2111

Mean 0.6 4 11.9

III trivalents; H bivalents

At early pachytene, basides one closed SC trivalent, one or two open SC trivalents can be seen in each spermatocyte. The other seven to eight trivalents are joined into multichro- mosomal chains by means of SCs formed between the short arms of acrocentrics of neighbouring trivalents (see next section).

In some completely paired trivalents, in which SCs are formed between the short arms of acrocentrics, gaps in the lateral element of the pericentromeric regions of the Rb metacentrics were observed occasionally (Fig. 4d). This in- dicates that gaps are not artefacts caused by spreading forces but reflect the process of slow axial element forma-

Fig. 6a-c . A surface-spread early pachytene spermatocyte, a The entire complement. B1-B 6 autosomal bivalents; X Y sex bivalents; T1 completely paired SC (synaptonemal complex) trivalent; T2-T6 incompletely paired SC trivalents with gaps (hollow arrowheads) in the lateral elements of metacentrics; TT-Ts a chain of two incompletely paired SC trivalents with similar gaps in the lateral elements; Tg-Tlo a chain of two completely paired SC trivalents with a thin and stretched lateral element of the metacentric in Tg. Solid arrowheads indicate SCs between short arms of acrocentrics connecting neighbouring trivalents into chains. The T7 Ts chain is illustrated in more detail in b. Bar represents 10 gm. b A chain of two incompletely paired SC trivalents (TT-Ts chain in a). A1, A'~, MI the axial elements of the first SC trivalent; Az, A~, M2 the axial elements of the second trivalent. The solid arrowhead indicates an SC segment formed between the short arms of the axial elements of the acrocentrics A] and A2. Gaps in the axial elements of the metacentrics are indicated by hollow arrowheads. Bar represents 1 gin. e A chain of two SC trivalents: A1, A'~, MI and A2, A'2, Mz from another spermatocyte. All designations are as in a. Bar represents I gin

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tion in Rb metacentrics, as is explained in the Discussion and in Figure 9 b-d.

Multichromosomal chains

In addition to completely and incompletely paired triva- lents, complex associations of SC trivalents - chains of tri- valents - were observed at late zygotene, early and mid pachytene (Figs. 5 and 8; Table 2). In many early and mid pachytene cells it was impossible to estimate the number of lateral elements in these chains due to entangled and discontinuous lateral elements. In some cases bivalents were included in chains. At least once we found a sex bivalent involved in such a chain (Table 1).

The linkage of trivalents into chains is achieved through short SCs forming between the short arms of nonhomolo- gous acrocentrics. The long arms of acrocentrics enter syn- apsis with lateral elements of homologous metacentrics as

' in an ordinary trivalent (Fig. 6c). The short arms appear to consist partially of heterochromatin as identified by C- banding. Thus, these arms may be at least partially homolo- gous to one another (Fig. 7). The eentromere-adjacent re- gions of lateral elements of metacentrics composing SC chains were always very much stretched and unpaired.

During early pachytene the lateral elements participat- ing in SC chains are often discontinuous. It can be seen from Table 2 that these nuclei contain a mean of 7 breaks per cell compared to 4.5 and 4 breaks per nucleus at the preceding and following stages. Such breakage can be found in pericentromeric regions of both metacentrics and acro- centrics participating in the chains. In some acrocentrics the short arm of the lateral element was broken. As a result, a chain of lateral elements dissociated into "pseudobiva- lents" each consisting of SCs in which one arm of a meta- centric and one acrocentric are paired (Fig. 6a, b). Such pseudobivalents are usually lying in line or at a slight angle to each other, facilitating the finding of the members of a pair of pseudobivalents originating from one trivalent. The broken ends of pseudobivalents are distinguishable from the telomeres by the lack of attachment plaques, and by the Y shape of the end with the break because of asynap- sis in the pericentromeric segments of the broken trivalent. Some of these breaks may have arisen from the resolution of interlockings (Holm and Rasmussen 1984; von Wettstein et al. 1984). As shown in Table 2, interlockings are formed at late zygotene, and some of them appear to be resolved prior to pachytene (Table 2). Table I shows also that nu- merous and long SC chains found at the late zygotene stage (24 lateral elements per cell on average) partially dissociated at the early and mid pachytene stages (11.3 and 11.9 lateral elements per cell on average, respectively). We should em- phasize that the number of chromosomes included in the chains was calculated irrespective of occasional breaks in their lateral elements. Dissociation of the chains into short- er ones depends not on breaks in the lateral elements but on true desynapsis of SCs of nonhomologous acrocentric elements connecting adjacent trivalents.

We found no late pachytene cells in animals no. 15 and 17. Four late pachytene cells were found in the cell spreads of animal no. 18. There were no chains of chromosomes in these cells (Table 1). Only eight completely formed triva- lents were observed in each cell together with four pseudobi- valents. Cells at diakinesis and metaphase I were not ob- served.

Fig. 7. C-banding pattern of Ellobius talpinus chromosomes with 2n = 54. The short chromosome arms contain C-heterochromatin

Discussion

The present study shows that the formation of SC trivalents in E. talpinus animals heterozygous for Rb translocations occurs in three ways. The first is complete pairing into triva- lents during zygotene when a short SC is formed between the short arms of acrocentrics (Fig. 9 a). Such early forma- tion of completely paired trivalents has not so far been described for other cases. Thus, Moses et al. (1979) have reported that the short arms of acrocentric chromosomes remain unpaired until pachytene.

Delayed pairing was only observed in some of the triva- lents. The lateral elements in the centromeric region of the metacentric chromosomes in such slowly forming trivalents remain indistinct for a long time and the short arms of the two acrocentrics are unpaired. The delay may be due to mechanical reasons if, for example, the telomeres of the short arms of acrocentrics are attached to the nuclear mem- brane on either side of the nucleus thus stretching the meta- centric (Fig. 9 b-d). The gaps in the metacentrics may also result from breakage during resolution of interlockings.

The third kind of trivalent formation is formation of chromosome chains composed of SC trivalents. These may later dissociate into individual trivalents. The linkage of trivalents in a chain is achieved through pairing between the short arms of nonhomologous acrocentrics (Fig. 9e) and implies the formation of SCs between C-heterochro- matic short arms of the acrocentrics. It is clear that the short arms of the acrocentrics in each trivalent are present in the monosomal state in cells heterozygous for the Rb translocation (Gropp and Winking 1981). These short arms of the acrocentrics may engage in nonhomologous synapsis. There are several cases which have been described which demonstrate that the monosomal or trisomal state of chro- mosomes in meiocytes inevitably results in nonhomologous Pairing. Such a phenomenon has been observed for univa- lents in Bombxy triploids (Rasmussen 1977) and in haploid plants in which all chromosomes are monosomal and form numerous nonhomologous SCs (Gillies 1974).

Short arms of acrocentrics in E. talpinus contain C-het- erochromatin (see Fig. 7) enriched in highly repetitive DNA (Ghinatulin et al. 1977). The presence of highly repeated DNA in these chromosomal regions may promote synapsis and formation of SCs between them, and substantial ho- mology may exist between these arms. Irrespective of the mechanisms underlying this pairing the formation of SCs

Fig. 8. A chain of trivalents. The dashed line connects the ends of a gap in the lateral dement designated Ms. All designations as in Figure 6. Bar represents 1 pm

IJIIIllPllli ~ ~ ' "

a M M 2 A' 1 e

b I M

/vl 1

d M

M2

Fig. 9a-f . Three schemes for SC trivalent formation in Ellobius talpinus F1 hybrids between animals with 2n = 54 and 2n = 34. a Direct formation of SC trivalents; A1, A'~ the axial elements of the acrocentrics; M the axial element of the Robertsonian metacentric, b, e, d Format ion of SC trivalents when the pericentromeric region of the lateral element of the Robertsonian metacentric is stretched due to a t tachment to two distantly located points of the inner nuclear membrane, e Format ion of chains of SC trivalents by means of SC segments (arrows) appearing between short monosomic heterochromatic arms of acrocentrics belonging to neighbouring SC trivalents, f Dissociation of chains of SC trivalents into free SC trivalents at late pachytene

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between monosomic heterochromatic short arms of acro- centrics in E. talpinus are regular phenomena resulting in the formation of trivalents and chains of trivalents. Such synapsis is subjected to correction in the course of pachy- tene. The main condition for successful correction is that crossing over does not fix multivalent combinations before they dissociate. In the case of E. talpinus this condition seems to be ensured because crossing over does not occur in short heterochromatic arms of acrocentrics: its absence in heterochromatin is a rule for many organisms (Stack 1984). It should be emphasized though that we discovered only a few cells at the late pachytene stage in which correc- tion of synapsis was completed by dissociating the SC chains into SC trivalents (see Table 1).

The fertility of E. talpinus animals heterozygous for ten Rb translocations is known to be reduced approximately two-fold (Lyapunova and Yakimenko 1985). A common opinion is that non-disjunction of the Rb trivalent is the primary reason for reduced fertility in Rb heterozygotes (Gropp and Winking 1981). It seems that the situation is more complex in E. talpinus heterozygous for numerous Rb translocations in which chains of trivalents are formed. Par- tial arrest of meiosis at pachytene because of a failure to resolve SC chains into discrete trivalents may be another reason for reduced fertility in the animals. The low fre- quency of spermatocytes at the late pachytene stage and the absence of post-pachytene stages in testes observed in the present study indicate such a causal relationship. Evi- dence for the arrest of spermatocyte development of semi- fertile and sterile mice carrying several Rb translocations has been published recently by Redi et al. (1985).

Ratomponir ina et al. (1984) have reported that in le- murs heterozygous for several Rb translocations chromo- somal chains have been observed in pachytene spermato- cytes. Such chains are also apparent in their previous inves- tigation of Rb translocation heterozygotes of lemurs (Moses et al. 1979). They give no explanations for the mech- anism underlying the development of chains, but it is highly probable that it is the same as in E. talpinus. They have proposed that such chains may contribute to reducing fertil- ity and this hypothesis requires further investigation.

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Received September 15, 1985 / in revised form April 4, 1985 Accepted by D. v. Wettstein