Synaptonemal complex analysis of an X-autosome translocation-carrier in the domestic pig

HAL Id: hal-00893938

https://hal.archives-ouvertes.fr/hal-00893938

Submitted on 1 Jan 1991

HAL is a multi-disciplinary open access

archive for the deposit and dissemination of

sci-entific research documents, whether they are

pub-lished or not. The documents may come from

teaching and research institutions in France or

abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est

destinée au dépôt et à la diffusion de documents

scientifiques de niveau recherche, publiés ou non,

émanant des établissements d’enseignement et de

recherche français ou étrangers, des laboratoires

publics ou privés.

Synaptonemal complex analysis of an X-autosome

translocation-carrier in the domestic pig

Daf Villagomez, M Świtoński, B Singh, Krs Fisher, I Gustavsson, Pk Basrur

To cite this version:

Synaptonemal

complex

analysis

of

an

X-autosome translocation-carrier

in the domestic

_pig

DAF

_Villagomez

M

&jadnr;wito&jadnr;ski

2

B

_Singh

₃

KRS

Fisher

3

I

Gustavsson

PK Basrur

3

1

Swedish University of Agricultural Sciences,

Department

of Animal Breeding

and

_{Genetics, Uppsala, Sweden;}

! Academy

of Agriculture, Department of

Genetics and Animals

Breeding,

Wolynska

33, 60-637

_{Poznan, Poland;}

3

University of Guelph,

Department

of

Biomedical

_{Sciences, Guelph,}

Canada

(Proceedings

of the 9th

_{European Colloquium}

on

_Cytogenetics

of Domestic

_Animals;

Toulouse-Auzeville,

10-13

_July

₁₉₉₀₎

synaptonemal complex analysis

/

X-autosome translocation

_/

domestic pig

Sporadic

cases of X-autosome translocations have been found in domestic animals

and,

recently,

Gustavsson et al

₍₁₉₈₉₎

_reported

the first

_finding

of such a translo-cation in the domestic

_pig.

The

_present

_{investigation}

deals with a

synaptonemal

complex

(SC)

analysis

by

electron

_microscopy

of another X-autosome translocation

in a sterile male

_pig,

which revealed meiotic arrest at the

_primary

_spermatocyte

level

_{(Singh, 1990).}

The translocation occurred

_proximally

in chromosome 14 and

terminally

in

_Xp

_{(fig la).}

In

_total,

57 _{spermatocytes} in the

_pachytene

_stage

were

_{investigated using}

the

technique

described earlier

_(Counce

and

_Meyer,

_1973).

The translocation chromo-somes formed 2 bivalents in 51 cells

(89.5%)

in which the axes of the Y and the

14q—

chromosomes were

_completely

_paired

into a bivalent

configuration

similar to

that of the normal autosomal bivalents

_(fig

_lb).

The bivalent was _easy to

iden-tify,

since it was the smallest SC

configuration.

The common association with a

chromocenter was also

easily

discernible. The second

bivalent,

consisting

of chro-mosomes 14 and

_Xp+,

was

heteromorphic

with axes of

_unequal

size. The

_longer

axis was formed

_by

the

Xp+,

with the

_unpaired

_segment

_appearing

stranded and

sometimes folded back and

_pairing

end-to-end with the free end of chromosome 14. Most often

_{(42 cells),}

the axis of chromosome 14 was

_{completely paired}

with chro-mosome

_Xp+,

which

_occasionally

_{(3 cells)}

_adjusted

its

_length

to become

_completely

out of

₅₇₎

exhibited end-to-end associations between the

unpaired

segment

of the

Xp+

axis and normal autosomal bivalents

_and,

in 9

_cells,

chromosome 14 showed such

_pairings.

In a small

_proportion

of cells

(10.5%),

the translocation

_product

was an _open

quadrivalent,

formed

_by

the association of either the free

_segment

of

_Xp+

(3 cells),

or the

_proximal

_segment

of chromosome 14

_{(3 cells),}

with the axis of either the Y chromosome or chromosome

_14q—,

_{respectively.}

Since there is no

_homology

between the

_unpaired

_segment

of chromosome

_Xp+

_(since

it

_belongs

to the q arm of the X

_chromosome)

and the Y

_chromosome,

the association observed should be

_{non-homologous}

_{(fig ld).}

There was

_only

one

_quadrivalent

in which

_pairing

of chromosome 14 with the centromeric end of

_14q-

led to central element formation.

Contrary

to the theoretical

_{expectations,}

the

present

aberration most

_frequently

formed 2 bivalents instead of a

_{quadrivalent. Nevertheless,}

_unequivocal

identifica-tion of the

_{pairing region}

of the sex chromosomes could be made

_{by correlating}

the

findings

from the somatic chromosome

analysis

with those of the

_synaptic

_analysis

of the translocation. Since the derivative chromosome

_{14q— always paired}

with the Y chromosome and the

_breakpoint

in X was observed

_distally

in the short _arm, it can be concluded that the X and Y

_pairing

_segment

lies

_distally

in the

_Xp

arm. At

_{early pachytene,}

the

_pairing

of the

_pig

sex chromosomes often includes the to-tal Y

_{(Schwarzacher}

et

al,

1984).

In the present

translocation,

the Y chromosome also

synapsed

completely

with chromosome

_14q—,

which had obtained its terminal

part

from the

_Xp

arm and conserved the centromeric

_region

of chromosome 14. The

_bivalent,

formed

_by

the Y chromosome and derivative

_14q-,

should be con-sidered a result of

_homologous

and

_{non-homologous}

_pairing.

The same should be true when chromosome 14 was

_{completely paired}

with chromosome

Xp+.

A similar

heterologous

synapsis

was observed in

heteromorphic

bivalents of 2 X-autosome

translocations

_(R5

and

_R6)

in male mice

_{(Ashley, 1983).}

In Gallus domesticus

_also,

cytological

evidence

_suggests

that ZW gonosomes

undergo non-homologous pairing

in Z-autosome translocations

_(Solari

et

_al,

_1988).

The formation of bivalents may

be due to

_{pairing competition.}

When the

Xp+

and the Y chromosomes are

com-pletely paired

with chromosome 14 and derivative

_14q—,

_{respectively,}

_they

_probably

prevent the

_pairing

of the latter two chromosomes and lead to a

_{high frequency}

of bivalent formation.

_Although

in some

_{spermatocytes}

₍₉

out of 57

_cells)

the heter-obivalent exhibited

_unpaired

_segments

of chromosome

_14,

the Y chromosome was

always

completely paired

with chromosome

_14q—.

_Finally,

it is clear that the

pair-ing

is

_{non-homologous}

in the _open

_{quadrivalents}

formed

_by

the association of the

Xp+

axis with the axes of the Y and chromosome

_14q—.

There is

_only

one

_previous

_report

of an X-autosome

_reciprocal

translocation in

the domestic

_pig

_(Gustavsson

et

_al,

_1989).

In that case as well as in the

_present

translocation,

the male was

_sterile,

which is a common

_phenomenon

in this type of translocation in man and mouse

(reviewed

_by

Mattei et

_{al, 1982; Searle,}

_1982).

REFERENCES

Ashley

T

₍₁₉₈₃₎

_{Nonhomologous synapsis}

of the sex chromosomes in the

_{heteromorphic}

bivalents of two X-7 translocations in male mice: R5 and R6. Chromosoma

_88,

178-183

Chandley

AC

₍₁₉₈₂₎

Normal and abnormal meiosis in man and other mammals. In: Serono

Clinical

_Colloquium

on

_Reproduction

_(Crosignani

PG et al,

eds)

Academic

_Press/Grune

& Stratton

Counce

SJ, Meyer

GF

₍₁₉₇₃₎

Differentiation of the

_{synaptonemal complex}

and the kinetochore in Locusta _{spermatocytes} studied

_by

whole mount electron

_microscopy.

Chrornosoma 44, 231-253

Gustavsson I,

Switonski

M,

lannuzzi _L, P16en L, Larsson K

₍₁₉₈₉₎

_Banding

studies and

synaptonemal complex analysis

of an X-autosome translocation in the domestic

_pig.

Cytogenet

Cell Genet 50, 188-194

Lifschytz E, Lindsley

DL

₍₁₉₇₂₎

The role of X-chromosome inactivation

_during

spermato-genesis.

Proc Natl Acad Sci USA 69, 182-186

Mattei

_MIG,

Mattei

_{JF, Ayne S,}

Giraud F

₍₁₉₈₂₎

X-autosome translocations:

_cytogenetic

characteristics and their consequences. Hum Genet

61,

295-309

Schwarzacher

_{T, Mayr B,}

Schweizer D

₍₁₉₈₄₎

Heterochromatin and nucleolus

_organizer

region

behavior at male

_pachytene

of Sus

_scrofa

domestica. Chromosoma

_91,

12-19 Searle AG

₍₁₉₈₂₎

The

_genetics

of

_sterility

in the mouse. In: Serorco Clinical

Colloquium

on

_Reproduction

(Crosignani

PG et

_al,

_eds)

Academic

_Press/Grune

& Stratton

Singh

B

₍₁₉₉₀₎

An X-autosome translocation in the

pig:

characterization and

impact

on

fertility.

Master’s

_{Thesis, University}

of

_{Guelph, Guelph, Ontario,}

Canada