Constitutive heterochromatin, consisting of repetitive sequences, diverges very rapidly; therefore, its nucleotide sequences and chromosomal distributions are often largely different, even between closely related species. The chromosome C-banding patterns of two Gerbillinae species, Meriones unguiculatus and Gerbillus perpallidus, vary greatly, even though they belong to the same subfamily. To understand the evolution of C-positive heterochromatin in these species, we isolated highly repetitive sequences, determined their nucleotide sequences, and characterized them using chromosomal and filter hybridization. We obtained a centromeric repeat (MUN-HaeIII) and a chromosome 13-specific repeat (MUN-EcoRI) from M. unguiculatus. We also isolated a centromeric/pericentromeric repeat (GPE-MBD) and an interspersed-type repeat that was predominantly amplified in the X and Y chromosomes (GPE-EcoRI) from G. perpallidus. GPE-MBD was found to contain a 17-bp motif that is essential for binding to the centromere-associated protein CENP-B. This indicates that it may play a role in the formation of a specified structure and/or function of centromeres. The nucleotide sequences of the three sequence families, except GPE-EcoRI, were conserved only in Gerbillinae. GPE-EcoRI was derived from the long interspersed nuclear elements 1 retrotransposon and showed sequence homology throughout Muridae and Cricetidae species, indicating that the repeat sequence occurred at least in the common ancestor of Muridae and Cricetidae. Due to a lack of assembly data of highly repetitive sequences constituting heterochromatin in whole-genome sequences of vertebrate species published to date, the knowledge obtained in this study provides useful information for a deep understanding of the evolution of repetitive sequences in not only rodents but also in mammals.

1.
Alhajeri
BH
,
Hunt
OJ
,
Steppan
SJ
.
Molecular systematics of gerbils and deomyines (Rodentia: Gerbillinae, Deomyinae) and a test of desert adaptation in the tympanic bulla
.
J Zool Syst Evol Res
.
2015
;
53
(
4
):
312
30
.
2.
Aniskin
VM
,
Benazzou
T
,
Biltueva
L
,
Dobigny
G
,
Granjon
L
,
Volobouev
V
.
Unusually extensive karyotype reorganization in four congeneric Gerbillus species (Muridae: Gerbillinae)
.
Cytogenet Genome Res
.
2006
112
1-2
131
40
.
3.
Baker
RJ
,
Kass
DH
.
Comparison of chromosomal distribution of a retroposon (LINE) and a retrovirus-like element mys in Peromyscus maniculatus and P. leucopus
.
Chromosome Res
.
1994
;
2
(
3
):
185
9
.
4.
Boyle
AL
,
Ballard
SG
,
Ward
DC
.
Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization
.
Proc Natl Acad Sci USA
.
1990
;
87
(
19
):
7757
61
.
5.
Burt
DW
,
Bruley
C
,
Dunn
IC
,
Jones
CT
,
Ramage
A
,
Law
AS
.
The dynamics of chromosome evolution in birds and mammals
.
Nature
.
1999
;
402
(
6760
):
411
3
.
6.
Capanna
E
,
Merani
MS
.
Karyotypes of somalian rodent populations. 2. The chromosomes of Gerbillus dunni (Thomas, 1904), Gerbillus pusillus (Petrers, 1878) and Ammodillus imbellis (de Winton, 1898) (Cricetidae Gerbillinae)
.
Italian J Zool
.
1981
;
14
(
1
):
227
40
.
7.
Cazaux
B
,
Catalan
J
,
Justy
F
,
Escudé
C
,
Desmarais
E
,
Britton-Davidian
J
.
Evolution of the structure and composition of house mouse satellite DNA sequences in the subgenus Mus (Rodentia: Muridea): a cytogenomic approach
.
Chromosoma
.
2013
;
122
(
3
):
209
20
.
8.
de la Fuente
R
,
Manterola
M
,
Viera
A
,
Parra
MT
,
Alsheimer
M
,
Rufas
JS
.
Chromatin organization and remodeling of interstitial telomeric sites during meiosis in the Mongolian gerbil (Meriones unguiculatus)
.
Genetics
.
2014
;
197
(
4
):
1137
51
.
9.
Dobigny
G
,
Granjon
L
,
Aniskin
V
,
Ba
K
,
Volobouev
V
.
Eine neue Zwillingsart von Taterillus (Muridae, Gerbillinae) aus West-Afrika (A new sibling species of Taterillus (Muridae, Gerbillinae) from West Africa)
.
Mammal Biol
.
2003
;
68
(
5
):
299
316
.
10.
Essers
J
,
de Stoppelaar
JM
,
Hoebee
B
.
A new rat repetitive DNA family shows preferential localization on chromosome 3, 12 and Y after fluorescence in situ hybridization and contains a subfamily which is Y chromosome specific
.
Cytogenet Cell Genet
.
1995
69
3-4
246
52
.
11.
Fátyol
K
,
Cserpán
I
,
Praznovszky
T
,
Kereső
J
,
Hadlaczky
G
.
Cloning and molecular characterization of a novel chromosome specific centromere sequence of Chinese hamster
.
Nucleic Acids Res
.
1994
;
22
(
18
):
3728
36
.
12.
Fukushi
D
,
Kuro-o
M
,
Shichiri
M
,
Obara
Y
,
Tsuchiya
K
.
Molecular cytogenetic analysis of the highly repetitive DNA in the genome of Apodemus argenteus, with comments on the phylogenetic relationships in the genus Apodemus
.
Cytogenet Cell Genet
.
2001
92
3-4
254
63
.
13.
Ferguson-Smith
MA
,
Trifonov
V
.
Mammalian karyotype evolution
.
Nat Rev Genet
.
2007
;
8
(
12
):
950
62
.
14.
Gamperl
R
,
Vistorin
G
.
Comparative study of G- and C-banded chromosomes of Gerbillus canpestris and Meriones unguiculatus (Rodentia, Gerbillinae)
.
Genetica
.
1980
52-53
1
93
7
.
15.
Gauthier
P
,
Hima
K
,
Dobigny
G
.
Robertsonian fusions, pericentromeric repeat organization and evolution: a case study within a highly polymorphic rodent species, Gerbillus nigeriae
.
Chromosome Res
.
2010
;
18
(
4
):
473
86
.
16.
Grain
BJ
,
Westerkam
WD
,
Harrison
AH
,
Nadler
JV
.
Selective neuronal death after transient forebrain ischemia in the Mongolian gerbil: a silver impregnation study
.
Neuroscience
.
1988
;
27
(
2
):
387
402
.
17.
Hamilton
MJ
,
Hong
G
,
Wichman
HA
.
Intragenomic movement and concerted evolution of satellite DNA in Peromyscus: evidence from in situ hybridization
.
Cytogenet Cell Genet
.
1992
;
60
(
1
):
40
4
.
18.
Hirning
U
,
Schulz
WA
,
Just
W
,
Adolph
S
,
Vogel
W
.
A comparative study of the heterochromatin of Apodemus sylvaticus and Apodemus flavicollis
.
Chromosoma
.
1989
;
98
(
6
):
450
5
.
19.
Hörz
W
,
Altenburger
W
.
Nucleotide sequence of mouse satellite DNA
.
Nucleic Acids Res
.
1981
;
9
(
3
):
683
96
.
20.
Iwasa
MA
,
Iwai
H
,
Kai
O
.
Karyological characterization of laboratory strains of Mongolian gerbils using differential staining techniques
.
Cytologia
.
2016
;
81
(
2
):
237
42
.
21.
Kalitis
P
,
Choo
KHA
.
The centromere
. In:
Choo
KHA
, editor.
Centromere DNA of Higher Eukaryotes
Oxford University Press
1997
. p.
97
142
.
22.
Kalscheuer
V
,
Singh
AP
,
Nanda
I
,
Sperling
K
,
Neitzel
H
.
Evolution of the gonosomal heterochromatin of Microtus agrestis: rapid amplification of a large, multimeric, repeat unit containing a 3.0-kb (GATA)11-positive, middle repetitive element
.
Cytogenet Cell Genet
.
1996
;
73
(
3
):
171
8
.
23.
Kamimura
E
,
Uno
Y
,
Yamada
K
,
Nishida
C
,
Matsuda
Y
.
Molecular cytogenetic characterization of C-band positive heterochromatin of the greater long-tailed hamster (Tscherskia triton, Cricetinae)
.
Cytogenet Genome Res
.
2022
;
162
(
6
):
323
33
.
24.
Kipling
D
,
Mitchell
AR
,
Masumoto
H
,
Wilson
HE
,
Nicol
L
,
Cooke
HJ
.
CENP-B binds a novel centromeric sequence in the Asian mouse Mus caroli
.
Mol Cell Biol
.
1995
;
15
(
8
):
4009
20
.
25.
Kirino
T
.
Delayed neuronal death in the gerbil hippocampus following ischemia
.
Brain Res
.
1982
;
239
(
1
):
57
69
.
26.
Kunze
B
,
Traut
W
,
Garagna
S
,
Weichenhan
D
,
Redi
CA
,
Winking
H
.
Pericentric satellite DNA and molecular phylogeny in Acomys (Rodentia)
.
Chromosome Res
.
1999
;
7
(
2
):
131
41
.
27.
Kuznetsova
IS
,
Prusov
AN
,
Enukashvily
NI
,
Podgornaya
OI
.
New types of mouse centromeric satellite DNAs
.
Chromosome Res
.
2005
;
13
(
1
):
9
25
.
28.
Marchal
JA
,
Acosta
MJ
,
Bullejos
M
,
Díaz de la Guardia
R
,
Sánchez
A
.
Sex chromosomes, sex determination, and sex-linked sequences in Microtidae
.
Cytogenet Genome Res
.
2003
101
3-4
266
73
.
29.
Masumoto
H
,
Masukata
H
,
Muro
Y
,
Nozaki
N
,
Okazaki
T
.
A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite
.
J Cell Biol
.
1989
;
109
(
5
):
1963
73
.
30.
Masumoto
H
,
Nakano
M
,
Ohzeki
J
.
The role of CENP-B and α-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres
.
Chromosome Res
.
2004
;
12
(
6
):
543
56
.
31.
Matsuda
Y
,
Harada
YN
,
Natsuume-Sakai
S
,
Lee
K
,
Shiomi
T
,
Chapman
VM
.
Location of the mouse complement factor H gene (cfh) by FISH analysis and replication R-banding
.
Cytogenet Cell Genet
.
1992
;
61
:
282
5
.
32.
Matsuda
Y
,
Chapman
VM
.
Application of fluorescence in situ hybridization in genome analysis of the mouse
.
Electrophoresis
.
1995
;
16
(
2
):
261
72
.
33.
Myers
P
,
Espinosa
R
,
Parr
CS
,
Jones
T
,
Hammond
GS
,
Dewey
TA
The Animal Diversity Web
.
2023
. Available from: https://animaldiversity.org.
34.
Modi
WS
,
Serdyukova
NA
,
Vorobieva
NV
,
Graphodatsky
AS
.
Chromosomal localization of six repeated DNA sequences among species of Microtus (Rodentia)
.
Chromosome Res
.
2003
;
11
(
7
):
705
13
.
35.
Neitzel
H
,
Kalscheuer
V
,
Henschel
S
,
Digweed
M
,
Sperling
K
.
Beta-heterochromatin in mammals: evidence from studies in Microtus agrestis based on the extensive accumulation of L1 and non-L1 retroposons in the heterochromatin
.
Cytogenet Cell Genet
.
1998
80
1-4
165
72
.
36.
Neitzel
H
,
Kalscheuer
V
,
Singh
AP
,
Henschel
S
,
Sperling
K
.
Copy and paste: the impact of a new non-L1 retroposon on the gonosomal heterochromatin of Microtus agrestis
.
Cytogenet Genome Res
.
2002
96
1-4
179
85
.
37.
O’Brien
SJ
,
Menninger
JC
,
Nash
WG
Atlas of Mammalian Chromosomes
Wiley
2006
. p.
174
.
38.
Ohki
I
,
Shimotake
N
,
Fujita
N
,
Jee
J
,
Ikegami
T
,
Nakao
M
.
Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA
.
Cell
.
2001
;
105
(
4
):
487
97
.
39.
Okura
Y
,
Arimoto
H
,
Tanuma
N
,
Matsumoto
K
,
Nakamura
T
,
Yamashima
T
.
Analysis of neurotrophic effects of hepatocyte growth factor in the adult hypoglossal nerve axotomy model
.
Eur J Neurosci
.
1999
;
11
:
4139
44
.
40.
Ouspenski
II
,
Brinkley
BR
.
Centromeric DNA cloned from functional kinetochore fragments in mitotic cells with unreplicated genomes
.
J Cell Sci
.
1993
105
Pt 2
359
67
.
41.
Pietras
DF
,
Bennett
KL
,
Siracusa
LD
,
Woodworth-Gutai
M
,
Chapman
VM
,
Gross
KW
.
Construction of a small Mus musculus repetitive DNA library: identification of a new satellite sequence in Mus musculus
.
Nucleic Acids Res
.
1983
;
11
(
20
):
6965
83
.
42.
Rossi
MS
,
Redi
CA
,
Víale
G
,
Massarini
AI
,
Capanna
E
.
Chromosomal distribution of the major satellite DNA of South American rodents of the genus Ctenomys
.
Cytogenet Cell Genet
.
1995
69
3-4
179
84
.
43.
Singh
AP
,
Henschel
S
,
Sperling
K
,
Kalscheuer
V
,
Neitzel
H
.
Differences in the meiotic pairing behavior of gonosomal heterochromatin between female and male Microtus agrestis: implications for the mechanism of heterochromatin amplification on the X and Y
.
Cytogenet Cell Genet
.
2000
91
1-4
253
60
.
44.
Singer
MF
.
Highly repeated sequences in mammalian genomes
.
Int Rev Cyt
.
1982
;
76
:
67
112
.
45.
Viegas-Péquignot
E
,
Derbin
C
,
Lemeunier
F
,
Taillandier
E
.
Identification of left-handed Z-DNA by indirect immunomethods in metaphasic chromosomes of a mammal, Gerbillus nigeriae (Gerbillidae, Rodentia)
.
Ann Genet
.
1982
;
25
(
4
):
218
22
.
46.
Viegas-Pequignot
E
,
Benazzou
T
,
Prod’Homme
M
,
Dutrillaux
B
.
Characterisation of a very complex constitutive heterochromatin in two Gerbillus species (Rodentia)
.
Chromosoma
.
1984
;
89
(
1
):
42
7
.
47.
Vieira-da-Silva
A
,
Adega
F
,
Guedes-Pinto
H
,
Chaves
R
.
LINE-1 distribution in six rodent genomes follow a species-specific pattern
.
J Genet
.
2016
;
95
(
1
):
21
33
.
48.
Volobouev
V
,
Lombard
M
,
Tranier
M
,
Dutrillaux
B
.
Chromosome-banding study in Gerbillinae (Rodentia). I. Comparative analysis of Gerbillus poecilops, G. henleyi and G. nanus
.
J Zool Syst Evol Res
.
1995
;
33
(
2
):
54
61
.
49.
Volobouev
V
,
Vogt
N
,
Viegas-Péquignot
E
,
Malfoy
B
,
Dutrillaux
B
.
Characterization and chromosomal location of two repeated DNAs in three Gerbillus species
.
Chromosoma
.
1995b
104
4
252
9
.
50.
Volobouev
V
,
Aniskin
VM
,
Sicard
B
,
Dobigny
G
,
Granjon
L
.
Systematics and phylogeny of West African gerbils of the genus Gerbilliscus (Muridae: Gerbillinae) inferred from comparative G- and C-banding chromosomal analyses
.
Cytogenet Genome Res
.
2007
;
116
(
4
):
269
81
.
51.
Wahrman
J
,
Richler
C
,
Neufeld
E
,
Friedmann
A
.
The origin of multiple sex chromosomes in the gerbil Gerbillus gerbillus (Rodentia: Gerbillinae)
.
Cytogenet Cell Genet
.
1983
;
35
(
3
):
161
80
.
52.
Wong
AKC
,
Rattner
JB
.
Sequence organization and cytological localization of the minor satellite of mouse
.
Nucleic Acids Res
.
1988
;
16
(
24
):
11645
61
.
53.
Xu
H
,
Miki
K
,
Ishibashi
S
,
Inoue
J
,
Sun
L
,
Endo
S
.
Transplantation of neuronal cells induced from human mesenchymal stem cells improves neurological functions after stroke without cell fusion
.
J Neurosci Res
.
2010
;
88
(
16
):
3598
609
.
54.
Yamada
K
,
Kamimura
E
,
Kondo
M
,
Tsuchiya
K
,
Nishida-Umehara
C
,
Matsuda
Y
.
New families of site-specific repetitive DNA sequences that comprise constitutive heterochromatin of the Syrian hamster (Mesocricetus auratus, Cricetinae, Rodentia)
.
Chromosoma
.
2006
;
115
(
1
):
36
49
.
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