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Genetics and Molecular Biology

Print version ISSN 1415-4757

Genet. Mol. Biol. vol. 21 n. 1 São Paulo Mar. 1998

http://dx.doi.org/10.1590/S1415-47571998000100012 

Centric fusion in goats (Capra hircus): Identification of a 6/15 translocation by high resolution chromosome banding

 

Lígia Souza Lima Silveira da Mota and Rosana Ap. Bicudo da Silva
Departamento de Genética, IB, Universidade Estadual Paulista (UNESP), Caixa Postal 529, 18618-000 Campus de Botucatu, SP, Brasil. Send correspondence to L.S.L.S.M.

 

 

ABSTRACT

Nine phenotypically normal Saanen goats (6 males and 3 females) belonging to the goat house of the Instituto de Biociências, UNESP, Botucatu Campus, were analyzed cytogenetically. The objective of the present study was to determine whether or not chromosomes 5 and 15 are involved in a Robertsonian translocation previously observed in a sample of a Brazilian herd using the chromosome pattern described by the ISCNDA (1989). The results suggest the involvement of chromosomes 6 and 15 in the fusion demonstrated by G-banding in prometaphase cells. The Brazilian sample of animals carrying structural rearrangements did not present any reduction in fertility, suggesting the existence of prezygotic selection against unbalanced gametes. Further investigations on the Brazilian herd are necessary to assess the real incidence of Robertsonian translocations and their effects on reproductive performance.

 

 

INTRODUCTION

The family Bovidae consists of various subfamilies, including the Bovinae and Caprinae which are of high economic interest. Cattle, sheep and goats present a high degree of similarity in terms of fundamental autosome number (FN = 58) (Buckland and Evans, 1978), chromosome banding pattern (Schnedl and Czaker, 1974; Mensher et al., 1989; Hayes and Petit, 1991; Iannuzi and Di Meo, 1995) and analysis of gene mapping (Chowdhary et al., 1991; Fernandez- Garcia et al., 1996). Karyotype evolution and speciation in this family seem to occur mainly by centric fusions (Wurster and Bernirschke, 1968).

The first studies on the occurrence of Robertsonian translocations in Saanen goats have been reported by Padeh et al. (1965, 1971), Soller et al. (1969) and Popescu (1972). Later studies using chromosome banding techniques allowed the identification of translocations that had occurred between chromosomes 5 and 15 (Evans et al., 1973; Jorge et al., 1987), t(6;17) (Elminger and Stranzinger, 1982) and t(6;15) (Burguete et al., 1987; Yang et al., 1990; Guillemot et al., 1993).

Cytogenetic information about other goat races is extremely limited. Dolf and Hediger (1984) and Moreno-Millan and Rodero-Franganillo (1990) reported the presence of a centric fusion in a male Toggenburg goat and in an intersex animal of the Malaguena race, respectively.

Morphological analysis of the translocated chromosomes by standard staining and comparison between the R- and G-banding patterns led various authors to suggest that the t(5;15), t(6;17) and t(6;15) reported in Saanen goats are identical (Burguete et al., 1987; Guillemot et al., 1991).

According to the International System for Cytogenetic Nomenclature of Domestic Animals (ISCNDA, 1989), the idiograms of the R- and G-banding patterns for cattle and goat chromosomes are similar, except for chromosomes 9, X and Y. Hayes and Petit (1991) performed high resolution RBG-banding pattern in goat, and later, Iannuzi and Di Meo (1995) improved this characterization by direct comparison with those of cattle and sheep. Recently, GTG-, GBG-, RBA- and RBG-banded prometaphase karyotypes with relative G- and R-banded idiograms have been reported for this species (Iannuzi et al., 1996). Therefore, the objective of the present study was to analyze a strain of a Brazilian Saanen goat herd in order to determine whether chromosomes 5 and 15 are involved in the translocation previously described in Brazil by Jorge et al. (1987), using the chromosome pattern described by the ISCNDA (1989).

 

MATERIAL AND METHODS

Characterization of the sample

In 1983, an intersex Saanen goat was sent to the Laboratory of Human and Animal Cytogenetics, Institute of Biosciences, UNESP, Botucatu Campus, by the Veterinary Hospital of the Faculty of Veterinary and Zootechnical Medicine, UNESP. This animal presented 2n = 59 chromosomes, with one chromosome showing submetacentric morphology. This finding encouraged the analysis of the other members of the genealogy (Jorge et al., 1987). Some animals were acquired, thus leading to the formation of the goat house of the Institute of Biosciences which, in 1987, consisted of 40 phenotypically normal animals carrying the translocation (36 heterozygotes and 4 homozygotes). The sire of this herd, a heterozygous carrier of the translocation, was the twin brother of the intersex animal (Oriani, 1987). A study of the geographic distribution of the translocation revealed that it was introduced into Brazil in 1979 by a male Saanen goat (Harald) imported from Switzerland (Gonçalves et al., 1992) and that the animals belonging to the goat house of UNESP were descendants of this sire.

Nine Saanen goats (6 males and 3 females) belonging to the above mentioned goat house were analyzed cytogenetically.

Cytogenetic analysis

Peripheral blood samples were drawn from the jugular vein and cultured according to the method described by Moorhead et al. (1960). The banding techniques employed in the present study included modifications of G- (Scheres, 1972) and high resolution banding (Rybak et al., 1982). Fifteen cells per animal were analyzed conventionally and when the presence of the centric fusion was confirmed 50 prometaphase cells per animal were karyotyped by G-banding. The chromosomes were identified and classified according to the ISCNDA (1989).

 

RESULTS

The chromosome complement of goats (Capra hircus) consists only of acrocentric chromosomes and therefore, even when using standard Giemsa staining, it was possible to identify animals that were heterozygous or homozygous carriers of centric fusions.

Cytogenetic studies performed on phenotypically normal goats revealed the presence of a Robertsonian translocation type (Figure 1). In prometaphase cells analyzed by GTG-banding, chromosomes 6 and 15 were found to be involved in the translocation according to the ISCNDA (1989) standard (Figure 2). The C-banding patterns (not shown) confirmed the dicentric nature of this translocation as earlier reported by Burguete et al. (1987).

 

Ms1857f1.gif (20940 bytes)

Figure 1 - Mitotic metaphase chromosomes of a male goat (Capra hircus) homozygous for the Robertsonian translocation visualized by standard Giemsa staining. Arrows indicate the translocated chromosomes.

 

 

Ms1857f2.gif (23287 bytes)

Figure 2 - Details of goat GTG-banded rob(6;15) drawn from different prometaphase cells homozygous for the translocation.

 

DISCUSSION

A summary of the translocations so far described in goats is shown in Table I. This type of rearrangement has been described since 1965; however, until 1971, the chromosomes involved had not been identified. Since 1973, with the advent of banding techniques, the translocations t(6;17) (Elminger and Stranzinger, 1982; Dolf and Hediger, 1984), t(6;15) (Burguete et al., 1987; Guillemot et al., 1993) and t(5;15) (Evans et al., 1973; Jorge et al., 1987) have been described.

 

Table I - Robertsonian translocations described in goats.

Race

Country

Number of animals carrying the translocation

Chromosomes involved

References

Saanen x UR* Israel

1

?

Padeh et al. (1965)
Saanen Israel

6

?

Soller et al. (1969)
Saanen Israel

38

?

Padeh et al. (1971)
UR* France

20

t(2;13)

Popescu (1972)
Saanen Scotland

1

t(5;15)

Evans et al. (1973)
Saanen Switzerland

3

t(6;17)

Elminger and Stranzinger (1982)
Saanen Germany

1

t(6;17)

Dolf and Hediger (1984)
Toggenburg Germany

1

?

Dolf and Hediger (1984)
Saanen Italy

7

t(6;15)

Burguete et al. (1987)
Saanen Brazil

59

t(5;15)

Jorge et al. (1987)
Malaguena Spain

1

t(10;12)

Moreno-Millan and Rodero Franganillo (1990)
Saanen France

1

t(6;15)

Guillemot et al. (1993)

*UR: Undefined race.

 

The inconsistency in the numeration of the translocated chromosome is mainly due to the lack of a standardization of the goat karyotype and to chromosome analysis restricted to metaphases when chromosomes are more condensed. The first standardization of the karyotype of this species was reported at the Reading Conference (1976). However, due to chromosome condensation the resolution of the banding pattern was very poor, especially in the case of smaller autosomes. Subsequently, such as in the ISCNDA (1989), the resolution of the banding pattern has been considerably improved and high resolution G- and R-banded karyotypes have been reported for cattle, especially when referring to the GTG-, QFQ- and RBA-banded ones. For goat, only RBA- and RBG-banded karyotypes have been reported. Later, several papers have reported high resolution G- and R-banding comparisons in goat (Iannuzi et al., 1994) as well as in goat, sheep and cattle (Iannuzi and Di Meo, 1995). More recently, Iannuzi et al. (1996) reported goat GTG-, GBG-, RBA- and RBG-banded prometaphase karyotypes with relative G- and R-banded idiograms. In the present study we used prometaphase chromosomes which are known to be more informative.

Morphological examination of the two chromosome arms stained by standard Giemsa suggests that the translocation presented here may be the same as described by Padeh et al. (1965) and, subsequently, by the other authors cited above. However, we cannot rule out the hypothesis that the translocation found in our sample, as well as in herds from other countries, may have occurred as an independent event. Although all combinations between acrocentric chromosomes are possible, the chromosomes involved in Robertsonian translocations do not participate in a random manner. Associations between satellites constitute a mechanism that may induce rearrangements between acrocentric chromosomes. However, these associations are not responsible for the participation of specific chromosomes in translocations (Jacob et al., 1976; Therman et al., 1989).

A cytogenetic study conducted by Gonçalves et al. (1992) on 205 animals revealed that 29.7% of the animals were heterozygous and 4.88% homozygous for t(5;15). Genealogical analysis showed that the animals carrying the centric fusion were descendants of a sire imported from Switzerland and identified to be heterozygous for the translocation (Jorge et al., 1987). We may state that the occurrence of this rearrangement, at least in Brazil, is due to the lack of cytogenetic selection in the imported goats.

Various questions about the possible relation between Robertsonian translocations and the phenotypic characteristics of domestic animals have arisen. During meiotic pairing the formation of a trivalent between the fused chromosome and its acrocentric homologues is observed in animals heterozygous for the translocation. The trivalent configuration can follow different directions, leading to the appearance of balanced or imbalanced gametes. This mechanism permits the formation of embryos with a normal, balanced or aneuploid chromosome complement. The latter case results in lethal genetic anomalies, therefore increasing the mortality rate of embryos. The occurrence of deleterious effects on goat prolificacy has been reported by Padeh et al. (1971).

Jorge et al. (1987) did not observe any effect of the translocation on fertility, weight at birth or reproductive indices. Therefore, these authors proposed the existence of a selective mechanism that prevents the participation of aneuploid gametes in gametogenesis. Guillemot et al. (1993) also did not observe any influence on reproductive performance of males carrying the translocation.

Amaral and Jorge (1994) analyzed the synaptonemal complex of 2 heterozygous males from the goat house of UNESP by electron microscopy and observed two homologous chromosomes, within a total of 50 nuclei, in cis configuration. This fact is considered to be a prerequisite for the development of balanced gametes.

In the present sample no reduction in animal fertility was observed. These results suggest the existence of a prezygotic selection against imbalanced gametes in such a way that the formation of aneuploid gametes is avoided. Cytogenetic investigations extended to the entire goat population are necessary in order to assess the real incidence of Robertsonian translocations in general and, in particular, the t(6;15) and its effects on reproductive performance.

 

ACKNOWLEDGMENTS

Publication supported by FAPESP.

 

 

RESUMO

Foram analisados citogeneticamente 9 caprinos (6 machos e 3 fêmeas) da raça Saanen, fenotipicamente normais, pertencentes ao capril do Instituto de Biociências, UNESP, campus de Botucatu. Objetivou-se, utilizando como padrão cromossômico o descrito em ISCNDA (1989), confirmar ou não o envolvimento dos cromossomos 5 e 15 na translocação Robertsoniana anteriormente observada em uma amostra do rebanho brasileiro. Os resultados sugerem o envolvimento dos cromossomos 6 e 15 na fusão analisada em células prometafásicas em bandamento G. A amostra brasileira de animais portadores de rearranjos estruturais não apresentou qualquer redução na fertilidade, sugerindo a existência de seleção pré-zigótica contra gametas não balanceados. A avaliação da real incidência das translocações Robertsonianas e seus efeitos no desempenho reprodutivo somente será possível com a ampliação das investigações no rebanho brasileiro.

 

 

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(Received November 3, 1997)