Synaptonemal complex analysis of reciprocal chromosome translocations in the domestic pig

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Synaptonemal complex analysis of reciprocal

chromosome translocations in the domestic pig

Daf Villagomez, I Gustavsson, L Plöen

To cite this version:

Synaptonemal complex analysis

of

_reciprocal

chromosome translocations

in the domestic

_pig

DAF

_Villagomez

I

Gustavsson

1

L Plöen

1

Swedish

_{University of Agricultural Sciences,}

Department of

Animal

_Breeding

and

Genetics;

and

2

Department of

Anatomy

and

_{Histology, Uppsala,}

Sweden

(Proceedings

of the 9th

_{European Colloquium}

on

_Cytogenetics

of Domestic

Animals;

Toulouse-Auzeville,

10-13

_July

₁₉₉₀₎

synaptonemal complex

analysis

/ reciprocal

chromosome

_{translocation}

_{/ domestic}

pig

One main feature of chromosome translocations in man and mouse is their common

association with meiotic

_impairment

of the carriers. This

_{happens especially}

when acrocentric chromosomes are involved and

_unpaired

_segments

of the translocation

configuration

are associated with the sex bivalent

_(Chandley,

1982;

Forejt,

1982).

In the domestic

_pig,

there is

_only

one indication that

_reciprocal

translocations

could lead to meiotic

_{degenerations}

_(Gustavsson

et

_al,

_1990).

We describe here the male

_{synaptonemal complex}

_(SC)

_behavior,

evaluated

_by

electron

_microscopy

and

prepared

according

to Counce and

_Meyer

_(1973),

of two

_reciprocal

translocations: rcp

(lq+/18q—)

and rcp

(7q+/17q—).

Both translocations resulted in one

_extremely

small derivative chromosome

_{(fig 1)}

and the

_{breakage/rejoining}

_points

of the involved chromosomes were localized

proximally

in the telocentric chromosomes

and

_terminally

in the q arm of the biarmed chromosomes.

Both boars were of the

_Hampshire

breed. The boar with rcp (lq+/18q-) had a

litter size decreased

_by

45%

in 15

litters,

but had a normal semen

_picture

and

no

_repeat

breeding;

there was one stillborn

_piglet.

The boar

_carrying

the _rcp

(7q+/17q—)

also had a normal semen

_picture

but the

_breeding

records showed a reduction of

41%

in the litter size

_along

with 3

repeat

breedings. Approximately

9%

of the liveborn

_piglets

died

_early

and most of them

_appeared

to be malformed.

Cytogenetic

investigations

showed that some of the malformed

_piglets

were

_tertiary

Fifty-seven

cells were

_investigated

at the

_pachytene

_stage.

With the

_exception

of

one

_spermatocyte

with two

_{heteromorphic}

_bivalents,

the

_remaining

56 cells demon-strated a

quadrivalent.

The most

_frequent

type of

_{configuration}

₍₂

_{early pachytene,}

12

_{mid-pachytene}

and 12 late

_pachytene

_cells)

was a

_completely

paired cross-shaped

quadrivalent morphology,

which involved some

_{non-homologous pairing}

of chromo-somes 1 and 18.

_{Completely paired quadrivalents}

without distinctive

_{heterosynapsis}

were found at mid- and late

_pachytene

₍₃

and 2

_cells,

_{respectively).}

This kind of

quadrivalent probably

reflects the

_{highest possible degree}

of

_homologous

pairing

(fig 2a).

Another common

_type

of

_morphology

observed was the buckle

configura-tion,

which could be classified into two

_categories.

One

_category

of buckle

quadri-valent

₍₃

cells at mid- and 13 cells at late

_pachytene)

showed remnants of central elements in the interstitial

_{unpaired region.}

The other

_type

of buckle

_quadrivalent

was without remnants of central elements in the

interstitially unpaired

segments

(2

early,

1 mid- and 4 late

_pachytene

_cells).

_Finally,

in two cells at

_{mid-pachytene,}

the

_quadrivalent

had the axes of the telocentric chromosomes

completely

unpaired.

The free ends were end-to-end associated with an autosomal bivalent.

The

_synaptic

behavior was

analyzed

in a total of 64 cells. Seven

spermatocytes

occurred when the axis of the derivative chromosome 17 was dissociated and when

there was no

heterosynapsis

between the normal chromosomes 7 and 17. A

univa-lent, ring-shaped

(1

cell)

and

_rod-shaped

_{(2 cells),}

was observed in 3 of the 4 cells

having

an _open trivalent. In the 3

_remaining

_zygotene

_cells,

2

_types

of

_quadrivalent

configurations

were found. An _open

_{quadrivalent,}

with the axis of chromosome

17q—

paired

either with chromosome number 7 or

_17,

was

_present

in 2

_cells,

and in one cell

chromosome

_17q—

was

_{partially synapsed}

with the 2 normal

chromosomes,

forming

a buckle

quadrivalent

configuration.

At

pachytene,

a

_variety

of

_{configurations}

were

formed.

_Fourty-seven

_(82.5%)

out of 57 cells showed a

_quadrivalent

configuration,

of which

only

11

_(23.4%)

had the

_{quadrivalent completely paired. Twenty-three}

(48.9%)

spermatocytes

with a

_quadrivalent

showed an _open

_{configuration,}

which

could be classified into 2

_types:

chromosome

_17q—

_synapsed

with chromosome 17

(7 cells),

and chromosome

_17q—

_synapsed

with chromosome 7

_{(16 cells).}

In both

types,

chromosomes 17 and

_7q

₊

were

_unpaired

to some _extent, which

_might

be due

to

_{non-homology.}

As

_expected,

most of chromosome 7

paired

with the

_homologous

segment

of chromosome

_7q+,

but also showed a short

_segment

available for

pair-ing

with chromosome

17q—.

Buckle

_{configuration}

was found in 13

spermatocytes,

which _may result from either

_{incomplete pairing}

in the interstitial

_regions

of the

quadrivalent

at

_{early pachytene}

or

_desynapsis

at mid-late

_{pachytene starting}

in these

_regions

of

_{completely paired quadrivalents. Eight}

cells had

_completely

paired

trivalents

_plus

a univalent

(axis

of chromosome

17q-)

but

_only

2

_{spermatocytes}

There was a clear difference in the

_pairing

behavior of the two translocations. The

rcp(lq+/18q-)

showed,

as

_{previously reported}

for several translocations in boars

(Gustavsson

et

_{al, 1988;}

Gabriel-Robez et

_al,

_1988),

a

_{regular synaptic}

behavior.

Quadrivalent

configurations

were most often found as well in

_{spermatocytes}

of the boar

_carrying

the

_{rcp(7q+/17q-),}

but many cells demonstrated dissociations. In both

_{translocations, completely}

_homologously

_paired

_{quadrivalents}

were less

frequent

than _any other class of

_{configurations.}

This _may be due to mechanical

problems

of

_pairing.

Another

_{possible explanation}

is that

_heterologous

_pairing

between the normal chromosomes involved in each translocation starts at the same

time as

_homologous

_pairing

of the translocation chromosomes. This is

supported

by

the fact

_that,

in both

_{translocations,}

buckle

quadrivalents

were seen most

_frequently

at the latest

_stages

_{of pachytene;}

some of them showed remnants of central elements.

Thus,

non-homologous

pairing

between the normal chromosomes could

_begin

at

early pachytene

followed

by

desynapsis

at

_{mid-pachytene}

not

_being

substituted

_by

homologous

pairing.

If the Miklos

_{(1974) hypothesis}

_applies

in the case of

_reciprocal

translocations in

_boars,

_early

_{heterosynapsis saturating}

the

_pairing

sites would be

a mechanism to avoid _germ cell loss.

The common occurrence of trivalent

_plus

univalent

(20.9%)

in the

rcp(7q+/17q—)

boar

_suggests

that the derivative element often was not bound

by

a chiasma. It is

_interesting

to note that the _open

_{quadrivalents}

showed more

dissociations of chromosome

17q-

from chromosome 17 than from chromosome 7

(17

and 8

cells,

respectively).

This

_finding

could be

explained

by

chiasmata

formed

more often

_{telomerically}

(segment

_pairing

with chromosome

7)

than

_{centromerically}

(segment

pairing

with chromosome

_17),

or that

_pairing

of chromosome

17q—

begins

preferably

at its distal end.

_Preliminary

_findings

in a

_tertiary

trisomic boar have

shown that the chromosome

_{17q— participates}

in a considerable number of

triva-lent

_formations,

most of which are due to

_pairing

with chromosome

_pair

7. Another

difference observed between the two translocations was the number of associations with the sex bivalent. In the

_{rcp(7q+/17q—)}

the translocation

_{configuration}

was

of-ten

_paired

or associated with the sex bivalent

(17.1%),

whereas no

_pairings

with the sex bivalent were seen in the

rcp(lq+/18q—).

According

to

_Lifschytz

and

_Lindsley

(1972),

association of

_unpaired

autosomal

_segments

with the sex chromosomes can

interfere with the X-inactivation which leads to breakdown of

_{spermatogenesis.}

It

should, however,

be noted that both carriers demonstrated a normal semen

_picture

and normal testicular

_histology.

REFERENCES

Chandley

AC

₍₁₉₈₂₎

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

Chromosoma 44, 231-253

Forejt

J

₍₁₉₈₂₎

XY involvement in male

_sterility

caused

_by

autosome translocations - a

hypothesis.

In: Serono Clinical

Colloquium

on

_Reproduction

_(Crosignani

PG et

_at,

_eds)

Gabriel-Robez

_0,

Jafar

_{H, Ratonponirina}

_C,

Boscher

_J,

Bonneau

J, Popescu

CP, Rumpler

Y

₍₁₉₈₈₎

_{Heterosynapsis}

in a

_heterozygous

fertile boar carrier of a _3;7 translocation.

Chromosoma 97, 26-32

Gustavsson I,

Switonski

M,

Larsson

K,

P16en

L, Hojer

K

₍₁₉₈₈₎

_{Chromosome-banding}

studies and

_{synaptonemal complex analyses}

of four

_reciprocal

translocations in the domestic

_pig.

Hereditas 109, 169-184

Gustavsson

_I,

Larsson

_K,

Switonski

M,

P16en L

₍₁₉₉₀₎

_Spontaneous

chromosome

translo-cation,

rcp(2;4)(pl7;qll),

in a boar

_{demonstrating impaired gametogenesis}

and decreased

litter size. Hereditas in _press

Lifschytz E, Lindsey

DL

₍₁₉₇₂₎

The role of X-chromosome inactivation

_during

spermato-genesis.

Proc Natl Acad Sci USA 69, 182-186