The chicken as a model to study microchromosomes in birds: a review

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The chicken as a model to study microchromosomes in

birds: a review

Valérie Fillon

To cite this version:

Review

The

chicken

as a

model

to

study

microchromosomes in

birds:

a

review

Valérie

Fillon

Laboratoire de

génétique cellulaire,

Institut national de la recherche

agronomique,

BP27,

31326 Castanet-Tolosan

_cedex,

France

(Received

17 December

1997; accepted

22

_April

₁₉₉₈₎

Abstract - The

typical

avian

_karyotype

is

_composed

of a few macrochromosomes

and around 60

indistinguishable

small microchromosomes. Due to its economic

importance,

the chicken is the avian

_species

for which

_cytogenetic

and

_genetic

_maps

are the most

developed.

Based on these _genome

_studies,

it has been shown that

the chicken microchromosomes are carriers of dense

_genetic

information.

_Indeed,

they probably

bear at least 50

%

of the genes and exhibit

_high

recombination

rates. Because of the _presence of

microchromosomes,

the

_genetic

size of the chicken

genome seems

_higher

than first estimated and could reach more than 4 000 cM

for 1 200 Mb.

Thus,

it is worth

_developing

the microchromosome _map. From an

evolutionary point

of

view,

comparative mapping

data raise many

questions

about

the

origin

of microchromosomes.

They

could be ancestral

_chromosomes,

from which

large

chromosomes formed

_{by fusions,}

or

_{conversely they}

could be the result of the

splitting

of

_{macrochromosomes. ©}

_{Inra/Elsevier,}

Paris

microchromosome

_/

chicken

_/

_{genomic map}

_/

recombination rate

Résumé - La Poule comme modèle d’étude des microchromosomes d’oiseaux :

une revue. Le

_caryotype

aviaire

_typique

est constitué de

_quelques

macrochromosomes

et d’environ soixante microchromosomes

punctiformes

et indiscernables les uns des

autres. Du fait de son

_{importance économique,}

la Poule est

_l’espèce

d’oiseaux dont les cartes

_génétique

et

cytogénétique

sont les

plus

avancées. Ces études ont

_permis

de montrer _que les microchromosomes contiennent une information

_génétique

dense.

En

_effet,

ils _portent

_probablement

au moins 50 % des

_gènes

et ils ont des taux de recombinaison élevés. Du fait de la

_présence

des

_{microchromosomes,}

la taille

_génétique

attendue pour le

génome

de la Poule est d’au moins 4 000 cM _pour 1200 Mb. Il

apparaît

donc

_important

de densifier la carte

_génétique

des microchromosomes. Du

point

de vue

_évolutif,

les données de

_{cartographie comparée}

soulèvent de nombreuses

questions

quant à

l’origine

des microchromosomes. Ils

_pourraient

être des caractères

ancestraux _ayant

_permis

la formation des

_grands

chromosomes _par

_fusion,

ou au

contraire être le résultat de

plusieurs

fissions

_{chromosomiques. @ Inra/Elsevier,}

Paris

microchromosome

_/

poule

/

carte

génomique

/

taux de recombinaison

INTRODUCTION

Microchromosomes were discovered in the first chicken chromosome

prepa-rations and were then considered as small

_genetically

inert accessory

_elements,

totally

heterochromatic,

without _{any gene} or centromere and

_constituting

a reserve of nucleic acids

for

chromosomal

replication

(57!.

Later

_{observations,}

demonstrating

their constant number in the

_karyotype

of different studied

species,

led to their

_being

considered as

_genuine

chromosomes

_[41,

58,

78],

although they

were

thought

to exhibit no recombination in order to _preserve ancestral

_linkage

groups

(73].

Birds are the vertebrates that have the

_greatest

number of microchromo-somes. The

_typical

avian

_karyotype

is

_composed

of around 80 chromosomes sep-arated into two classes: a few

_{distinguishable}

macrochromosomes and a much

higher

number of small

_{microchromosomes,}

visualized as dots on

_metaphase

preparations

and

_usually

classified

_by

_decreasing

size

_(17!.

_Except

for the

Fal-coniformes

and

_particularly

the

_{Accipitridae family}

which has no more than

three

to six microchromosome

pairs

_(24!,

the average

number

of microchromo-somes is 60

[17, 77!.

_Depending

on the

_species,

the borderline between both

groups is not

_always

clear. The usual criteria used to define microchromosomes are

_mainly

their size

_(which

varies

_according

to authors between 0.5 and 1.5

_u.m

(44!),

the

_{impossibility}

of

_{distinguishing}

them from each other and of

_defining

the centromere

_position

_(77!.

Because of its economic

importance,

the chicken is the avian

_species

for which

_cytogenetic

and

_genetic

maps are the most

_developed

and

_important

international efforts are under _way to build up a

complete

_{genome coverage,}

making

it a reference for the detailed

study

of bird _genomes.

2. THE CHICKEN KARYOTYPE

Although

the

_boundary

between macro- and microchromosomes varies

ac-cording

to

_authors,

the actual standard

_{karyotype description by}

GTG- and

RBG-banding

for

the

_chicken,

established

_by

the International

Committee

for the

Standardization

of the

Avian

_Karyotype,

concerns

eight

_pairs

of macrochromosomes and sex chromosomes Z and W

(ICSAK,

1993: K.

_Ladjali,

J.J.

_Bitgood,

R.N. Schoffner and F.A. Ponce de

_Leon;

_[42]).

The

_remaining

30

_pairs

of chromosomes are

referred

to as microchromosomes and

_only

an

approximate

size can

_usually

be

_given

for individual

_{descriptions. Indeed,}

due to their smaller size and lower

_degree

of chromatin

_compaction

_(68],

it is

im-possible

to obtain characteristic

_banding

patterns

for each

_pair.

However,

by

using

DAPI or

_chromomycin

A3

_staining,

it has been

_suggested

that most

the chicken _genome and determination of the

position

of the centromeres. Most microchromosomes were thus found to be acrocentric

_(37].

The

_physical

size of the chicken _{genome is 1 200} Mb: the mean size for chicken macrochromosomes

is around 130

_Mbases,

and

_only

12.5 Mbases for

microchromosomes,

with the smallest one estimated to be as small as 7 Mbases

(6!.

3. THE CHICKEN GENOMIC MAP

Chicken

_genetic

maps are

composed

of around 650 molecular markers

[13,

43!.

The

_genetic

size is between 2 500 and 3 400 cM.

_They

are

_composed

of a small number of

_{large linkage}

groups that have been

assigned

to macrochromo-somes, and numerous small

linkage

_groups or

independent

markers

probably

corresponding

to

_{microchromosomes,}

but for which a

_cytogenetic

localization still needs to be

defined

_[7,

9, 13,

15,

21,

43].

Recognizing

each individual

mi-crochromosome is essential to allow a

_precise

localization of _genes and

markers,

leading

to

_completed

_genetic

_maps. For this _purpose, a collection of

large

insert

BAC

_(bacterial

artificial

_chromosome)

and

PAC

_{(bacteriophage}

PI artificial

chromosome)

clones

_[80]

to be used as microchromosome

_tags

for identification

in two-colour FISH

_experiments

has been

developed

[29]

enabling

the individual characterization of 16 microchromosome

_pairs.

These clones have also

permit-ted 14

_linkage

_group

_assignments

_(Morisson,

_pers.

_comm.).

The identification of microchromosome

pairs

leading

to the

integration

of the

_genetic

and

cytoge-netic maps is the first

_step

towards a better

_knowledge

of

microchromosomes,

especially

with

_regards

their

_{genetic composition}

and their recombination rates.

4. THE

GENETIC COMPOSITION

OF

MICROCHROMOSOMES

4.1. The

_density

of genes

Despite

their _very small

_size,

microchromosomes seem to hold many genes.

CpG

islands,

which are short

unmethylated

CpG-rich

_sequences located towards the 5 end of many vertebrate genes

[1],

are enriched on microchro-mosomes

_[47].

This

_suggests

the _presence of a

_higher

_gene

_density

than on macrochromosomes.

Indeed,

more than half of the

mapped

_genes have been localized on chicken

_{microchromosomes,}

confirming

their

_{genetic importance}

[62],

whereas less than 40

%

of the

_genetically

_mapped

_genes are localized on macrochromosomes 1-4 which

_represent

50

%

of the chicken genome

[Chick

GBase

_{(http://www.ri.bbsrc.ac.uk/chickmap/chickgbase/chickgbase.html)!.}

_].

Moreover,

it has been demonstrated for a few _genes that the size of chicken intronic _sequences is shorter than for human

_homologues

_{[32, 34!.}

Microchro-mosome 16 confirms this

_{high density}

of _genes as it carries the

rDNA

_genes

_(2!,

major histocompatibility complexes

B

_{[5, 26]}

and

_{R f p-Y}

_(28!,

the lectin _genes

[4]

and a

few

other genes

(ChickGBase).

This

high

gene

density

demonstrates that it is worth

_developing

the

_genetic

_map of microchromosomes.

4.2. The distribution of

_repeated

sequences

especially

microchromosomes

lack

_repetitive

DNA

because of loss or

non-acquisition

of such _sequences.

_However,

constitutive heterochromatin is located

essentially

on chromosomes Z or W and some

microchromosomes,

whereas macrochromosomes are

_weakly

stained in

_C-banding

studies

[11,

_61,

74].

Moreover,

repeated

sequences enriched on microchromosomes have been cloned. The first one, isolated from

chicken,

represents

10

%

of the genome and

probably

concerns centromeric heterochromatin

_(45].

The second

_corresponds

to

5

%

of the

turkey

genome and is located on one third of the microchromosomes

(46J.

Some clones

_{showing repeated hybridization}

patterns

localized

_specifically

on microchromosome

_pairs

have also been

_reported

(29J.

_{Thus, despite}

their

high

gene

density

and their small

size,

microchromosomes do not lack

repeated

DNA.

Microsatellites are

_repeated

_sequences of

_particular

value for _genome

map-ping

as

_they

have been shown to be

_{highly polymorphic}

in the

chicken

_{[14, 18J.}

But the

_frequency

of

different

types

of microsatellites differs between birds and mammals. The

_frequency

of dinucleotides

_(CA)n

in birds is one fifth of that in

mammals.

There are 7 000-9 000

_(CA)n

in the chicken _genome,

_spread

_every 136-150

_kb,

instead of every 30 kb in human

[53, 65J.

Moreover, they

seem to be concentrated on macrochromosomes based on

PRINS

_experiments

(65].

The low

proportion

of

_(CA)n

in the chicken genome was confirmed

by high

_stringency

screening

of

PAC

and

BAC

libraries

_(Morisson,

_pers.

_comm.).

_However,

about one third of these clones were localized on microchromosomes

by FISH,

sug-gesting homogeneous

distribution of

_(CA)n

microsatellites between macro- and microchromosomes. It would be

_interesting

to screen for tri- or tetra-nucleotide

repeats

as

_they

seem more

_frequent

in _{the chicken genome}

_(53J.

5. THE RECOMBINATION RATE

OF

MICROCHROMOSOMES

At

least one chiasma _per chromosome is needed

regardless

of its size

[12,

27,

36J.

Indeed,

chiasma

_analyses

on chicken

_lampbrush

chromosomes demon-strated that in microchromosomes one or two

_{crossing-over}

events _may

oc-cur: on _average one per 11-12

Mb,

whereas avian macrochromosomes have one

crossing-over

per 30 Mb

[66,

69,

70J.

Despite

their small

size,

microchromosomes

would thus have an associated

linkage

_group of at least 50 cM and therefore a

high

genetic

to

_physical

distance ratio.

_Thus,

the two

_genetically

_independent

major

histocompatibility complexes

B and

_{R f p-Y}

_{[51, 52]}

have been

located

on the same microchromosome

_16,

_{demonstrating}

the occurrence of

recombi-nations

_(28J.

_Moreover,

based on

_mapping

of _anonymous molecular

_markers,

it

has

_recently

been shown in several cases that the

_linkage

groups

corresponding

to microchromosomes are more than 50 cM

_long

(Morisson,

_pers.

comm.).

Due to the _presence of

_{microchromosomes,}

but also because of the

_great

number of

_chromosomes,

the recombination

_potential

of the chicken _{genome is}

high.

Indeed,

the

_segregation

of

_parental

chromosomes

_during

meiosis allows a

_mixing

of

the

_genetic

material. The recombination index

(RI)

calculated

(RI

= n +

TC,

where n is the number of bivalents and TC the total number of

_chiasmatas)

is 90-100 in

_birds,

whereas it is on _average 50 in mammals

[68].

Moreover,

the domestic

_species

studied

_(dog,

_cat,

_{pig, cattle,}

_etc.)

tend

intense selection effort on small livestock

_populations

sometimes

_changing

allelic associations between

_closely

linked genes, and

creating

new

haplotypes.

According

to the values found in the

_chicken,

the

_potential

_response of avian genomes to selection could be very

high.

However,

if the recombination rate is

very

high,

saturated

_genetic

_maps would be _necessary to have very close markers

available each time in

order

to

_permit

a molecular marker-assisted selection. The current

_genetic

_maps contain around 650

genetic

markers

_[13].

However,

the _{genome coverage is} not achieved as 10

%

of new

_mapped

markers are still unlinked.

_Moreover,

the

_genetic

size of microchromosomes is

_high

_compared

to

their

_physical

size. We _may still

_expect

a total

_genetic

size as

large

as 4 000 cM for 1 200 Mb.

_Thus,

to detect

_QTL

_S

_,

1000-1200 markers will be needed on the map, so as to be able to choose a

_{high quality}

subset of 200-400 markers

[20, 21].

Thus,

more molecular markers should be

_{developed, especially}

for microchromosomes.

6. THE

EVOLUTIONARY

MEANING

OF

MICROCHROMOSOMES

Some

_regions

of

conserved

_syntenies,

_involving

2-6

_loci,

have

_already

been described between birds and

_{mammals, although they}

_diverged

some 300 mil-lion years ago

[9, 10].

Most of them concern macrochromosomes. For

_example,

chicken

chromosome 1

_corresponds

to human chromosomes

_{11, 12,}

15 and 17

[40],

and some _{genes of the chicken chromosome}

_7q

are conserved on human chromosome

_2q

_{[31, 33].}

Two cases

_involving

chicken microchromosomes have also been

_reported.

The first

_syntenic

group is

composed

of

three _genes

_{[35, 67]}

located on a 25-Mb microchromosome and on human chromosome

15q,

proba-bly

in the same order

_[35].

The second

_example

shows that human chromosome

17q corresponds

to at least four chicken

_chromosomes,

_including

chromosome Z

[19, 38],

chromosome 1

_[72]

and two different microchromosomes

_[60].

This

sug-gests

that numerous

_{rearrangements}

have occurred and raises

_interesting

ques-tions about the evolution of vertebrate _genomes, such as whether the microchro-mosomes

_originate

from

_{splitting large}

chromosomes or the macrochromosomes

originate

from

_aggregation

of small ones. Microchromosomes _{may contain} syn-tenic _groups well conserved within vertebrates.

Avian

microchromosomes may

represent

ancient genome structures that have

_aggregated

_together

in other

species

to

_give

rise

_through

evolution to

_larger

structures. If

_they

have not been

_rearranged

with other chromosomes

_during

avian

_evolution,

_{they might}

carry ancient gene combinations and their

study

would

_{give insights}

into the

general

evolution of

vertebrate

_karyotypes.

The _{current progress} in

_mapping

chicken _genes will

_generate

more

_{comparative mapping data,}

and will enable us to test this

_hypothesis

_by

further

_estimating

the

_degree

of

_{rearrangements}

between mammals and birds.

Microchromosomes are also

_present

in lower numbers in a few other verte-brates

_(fish,

_batracians,

_reptiles)

and tend to

_{disappear completely}

in mam-mals

_[68].

_According

to Rodionov

_[68],

it

_might

be

_tempting

to consider them as ancestral

chromosomes

_{although they}

are _very rare in fish and

batracians.

Indeed, they

could have been inherited from a common ancestor of the

bird

_karyotypes

seem _very well conserved between ratites and carinatas

_!17!.

The _appearance of microchromosomes could

_precede

bird

_adaptative

radia-tion at the

end

of the

Jurassic,

beginning

of the

Cretaceous

_[16].

However,

crocodilians

_!39!,

which are closer to

_birds,

have

_karyotypes

without _any

mi-crochromosome,

as do

_frogs

_[54].

In

_reptiles

_[48,

_64,

_76]

and

_amphibians

_[55],

only

a small number of chromosomes can be

thought

to be microchromosomes. We note as well that most

of

the bird

_species

show a

_{typical karyotype}

with around 60

microchromosomes,

although

the

_Accipitridae

have

_only

three to six

_pairs

of microchromosomes

_[22,

_23,

_24].

In

_{Ciconiiformes,}

there is an

im-portant

reduction in the number of chromosomes

_(50-60)

and

_only

around 20 microchromosomes

_{[3, 25!.}

Furthermore,

there is an increase in the number of chromosomes and microchromosomes in the

_{Coraciiformes,}

where more than 100 microchromosomes are found

[17, 77!.

At the current level of

_knowledge,

there are no data to

_explain

the

_high

num-ber of microchromosomes in bird

_karyotypes.

If it is the ancestral

_situation,

we could

_imagine

that mammalian chromosomes have been formed

_by

the fusion of microchromosomes

_and/or

the

_acquisition

of

_non-coding

DNA _sequences. When the number of macrochromosomes

_increases,

the number

of

microchromosomes

diminishes;

higher

proportions

of

acrocentric chromosomes are found in

_species

with

_larger

numbers of

_{microchromosomes,}

and more metacentric or submeta-centric macrochromosomes are found in

_species

with fewer microchromosomes

!77!.

Robertsonian fusions or translocations could occur between

_chromosomes,

leading

to the

formation

of two _very distinct groups of chromosomes

[44,

68,

77!.

The presence of many

telomeric,

pericentromeric

or

_interspersed

_sequences in the chicken genome could be the evidence for such chromosomal

rearrange-ments

_(56].

_However,

some

_species

(among Passeriformes)

have

_only

a telomeric distribution of

_(TTAGGG)n

sequences

(50!.

This sequence, very well conserved in

_vertebrates,

is located on _every

_telomere,

which is also true for microchro-mosomes

[49].

In

_reptiles,

fish and

_{amphibians, hybridization signals}

were also found in

_{pericentromeric}

or interstitial

_regions

for some

_species

[50].

But mi-crochromosomes could also be the result

of

chromosome

_fissions,

in which case

(TTAGGG)n

interstitial sites would be

interpreted

as

_{being regions existing}

prior

to the formation of new telomeres

!50!.

7. CONCLUSION

Microchromosomes are

_genuine

chromosomes,

probably bearing

at least 50

%

of the _genes in the chicken and

_{exhibiting high}

recombination rates. It makes sense to

_approach

the chicken genome

by

developing

the

genetic

map

of microchromosomes. Microsatellite sequences seem to be

_{uniformly spread}

within the _genome, and could

_provide

new molecular markers even if

_they

are less

_frequent

than

in

mammals.

Although

microchromosomes carry dense

genetic

information,

they

also have several families

_{of repeated}

DNA _sequences. Further studies on

_specific

chromo-some

_repeated

_sequences could

_give

valuable information on the

_organization

Despite

all the

_comparative

data

_available,

it is still difficult to understand the

_evolutionary

_meaning

of microchromosomes. The presence of conserved

segments

in mammals and birds allows the reconstitution of some chromosome

rearrangements

and the

_discovery

of

_probably

_{ancient groups of genes.} The

re-maining question

is the direction of chromosome evolution. Microchromosomes could be

_ancestral,

at the

_origin

of

_large

chromosomes

_by

fusion or

_conversely

originate

from macrochromosomes

_{by splitting.}

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Lambrou

M.,

Schleger W.,

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R.H.R.,

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L.E.M.,

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