Tandem repetitive sequences represent a significant part of many genomes but remain poorly characterized due to various methodological difficulties. Here, we describe the tandem repeat composition in the genome of zebra finch, Taeniopygia guttata, a species that has long served as an animal model, primarily in neurobiology and comparative genomics. Using available genome sequencing raw read datasets, we bioinformatically reconstructed consensus sequences of several tandem repeats and proved that the most abundant ones, Tgut191A and Tgut716A, are centromere-associated in chromosomes. Each centromeric region can have a different number of copies of each repeat, with Tgut716A enrichment in almost all microchromosomes and sex chromosomes. Sequences similar to Tgut191A and Tgut716A found in other Estrildidae and Viduidae species can be considered as candidate centromeric sequences, but this requires further cytogenetic verification.

1.
Achrem
M
,
Szućko
I
,
Kalinka
A
.
The epigenetic regulation of centromeres and telomeres in plants and animals
.
Comp Cytogenet
.
2020
;
14
(
2
):
265
311
.
2.
Ahmad
SF
,
Singchat
W
,
Jehangir
M
,
Suntronpong
A
,
Panthum
T
,
Malaivijitnond
S
,
Dark matter of primate genomes: satellite DNA repeats and their evolutionary dynamics
.
Cells
.
2020
;
9
(
12
):
2714
.
3.
Aird
D
,
Ross
MG
,
Chen
WS
,
Danielsson
M
,
Fennell
T
,
Russ
C
,
Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries
.
Genome Biol
.
2011
;
12
(
2
):
R18
.
4.
Atema
E
,
Mulder
E
,
Dugdale
HL
,
Briga
M
,
van Noordwijk
AJ
,
Verhulst
S
.
Heritability of telomere length in the zebra finch
.
J Ornithol
.
2015
;
156
(
4
):
1113
23
.
5.
Balzano
E
,
Giunta
S
.
Centromeres under pressure: evolutionary innovation in conflict with conserved function
.
Genes (Basel)
.
2020
;
11
(
8
):
912
.
6.
Bao
W
,
Kojima
KK
,
Kohany
O
.
Repbase Update, a database of repetitive elements in eukaryotic genomes
.
Mob DNA
.
2015
;
6
:
11
.
7.
Biltueva
LS
,
Prokopov
DY
,
Makunin
AI
,
Komissarov
AS
,
Kudryavtseva
AV
,
Lemskaya
NA
,
Genomic organization and physical mapping of tandemly arranged repetitive DNAs in sterlet (Acipenser ruthenus)
.
Cytogenet Genome Res
.
2017
;
152
(
3
):
148
57
.
8.
Boman
J
,
Frankl-Vilches
C
,
Dos Santos
M
,
de Oliveira
E
,
Gahr
M
,
Suh
A
.
The genome of blue-capped cordon-bleu uncovers hidden diversity of LTR retrotransposons in zebra finch
.
Genes
.
2019
;
10
(
4
):
301
.
9.
Capriglione
T
,
De Santo
MG
,
Odierna
G
,
Olmo
E
.
An alphoid-like satellite DNA sequence is present in the genome of a lacertid lizard
.
J Mol Evol
.
1998
;
46
(
2
):
240
4
.
10.
Choo
KHA
.
The Centromere
.
Oxford, New York
:
Oxford University Press
;
1997
.
11.
Deryusheva
S
,
Krasikova
A
,
Kulikova
T
,
Gaginskaya
E
.
Tandem 41-bp repeats in chicken and Japanese quail genomes: FISH mapping and transcription on lampbrush chromosomes
.
Chromosoma
.
2007
;
116
(
6
):
519
30
.
12.
Dos Santos
MD
,
Kretschmer
R
,
Frankl-Vilches
C
,
Bakker
A
,
Gahr
M
,
O´Brien
PCM
,
Comparative cytogenetics between two important songbird models: the zebra finch and the canary
.
PLoS One
.
2017
;
12
(
1
):
e0170997
.
13.
Earnshaw
WC
,
Rothfield
N
.
Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma
.
Chromosoma
.
1985
;
91
(
3-4
):
313
21
.
14.
Edwards
NS
,
Murray
AW
.
Identification of Xenopus CENP-A and an associated centromeric DNA repeat
.
Mol Biol Cell
.
2005
;
16
(
4
):
1800
10
.
15.
Farré
M
,
Narayan
J
,
Slavov
GT
,
Damas
J
,
Auvil
L
,
Li
C
,
Novel insights into chromosome evolution in birds, archosaurs, and reptiles
.
Genome Biol Evol
.
2016
;
8
(
8
):
2442
51
.
16.
Gamba
R
,
Fachinetti
D
.
From evolution to function: Two sides of the same CENP-B coin?
Exp Cell Res
.
2020
;
390
(
2
):
111959
.
17.
Hamilton
GE
,
Davis
TN
.
Biochemical evidence for diverse strategies in the inner kinetochore
.
Open Biol
.
2020
;
10
:
200284
.
18.
Ishishita
S
,
Tsuruta
Y
,
Uno
Y
,
Nakamura
A
,
Nishida
C
,
Griffin
DK
,
Chromosome size-correlated and chromosome size-uncorrelated homogenization of centromeric repetitive sequences in New World quails
.
Chromosome Res
.
2014
;
22
(
1
):
15
34
.
19.
Itoh
Y
,
Arnold
AP
.
Chromosomal polymorphism and comparative painting analysis in the zebra finch
.
Chromosome Res
.
2005
;
13
(
1
):
47
56
.
20.
Itoh
Y
,
Kampf
K
,
Arnold
AP
.
Molecular cloning of zebra finch W chromosome repetitive sequences: evolution of the avian W chromosome
.
Chromosoma
.
2008
;
117
(
2
):
111
21
.
21.
Jennings
WB
,
Edwards
SV
.
Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees
.
Evolution
.
2005
;
59
(
9
):
2033
47
. .
22.
Knief
U
,
Forstmeier
W
.
Mapping centromeres of microchromosomes in the zebra finch (Taeniopygia guttata) using half-tetrad analysis
.
Chromosoma
.
2016
;
125
(
4
):
757
68
.
23.
Komissarov
AS
,
Galkina
SA
,
Koshel
EI
,
Kulak
MM
,
Dyomin
AG
,
O'Brien
SJ
,
New high copy tandem repeat in the content of the chicken W chromosome
.
Chromosoma
.
2018
;
127
(
1
):
73
83
.
24.
Korlach
J
,
Gedman
G
,
Kingan
SB
,
Chin
C-S
,
Howard
JT
,
Audet
J-N
,
De novo PacBio long-read and phased avian genome assemblies correct and add to reference genes generated with intermediate and short reads
.
Gigascience
.
2017
;
6
(
10
):
1
16
.
25.
Krasikova
A
,
Fukagawa
T
,
Zlotina
A
.
High-resolution mapping and transcriptional activity analysis of chicken centromere sequences on giant lampbrush chromosomes
.
Chromosome Res
.
2012
;
20
:
995
1008
.
26.
Kulak
M
,
Takki
O
,
Galkina
S
.
Cell culture establishment from zebra finch embryonic fibroblasts
.
Adv Anim Vet Sci
.
2021
;
9
(
3
):
344
7
.
27.
Kuznetsova
IS
,
Thevasagayam
NM
,
Sridatta
PSR
,
Komissarov
AS
,
Saju
JM
,
Ngoh
SY
,
Primary analysis of repeat elements of the Asian seabass (Lates сalcarifer) transcriptome and genome
.
Front Genet
.
2014
;
5
:
223
.
28.
Ladjali-Mohammedi
K
,
Bitgood
JJ
,
Tixier-Boichard
M
,
Ponce De Leon
FA
.
International system for standardized avian karyotypes (ISSAK): Standardized banded karyotypes of the domestic fowl (Gallus domesticus)
.
Cytogenet Cell Genet
.
1999
;
86
(
3-4
):
271
6
.
29.
Liu
GE
,
Hou
Y
,
Brown
T
.
Analysis of CR1 repeats in the zebra finch genome
.
Systemics Cybernetics Informatics
.
2013
;
11
(
3
):
66
71
.
30.
Madsen
CS
,
Brooks
JE
,
de Kloet
E
,
de Kloet
SR
.
Sequence conservation of an avian centromeric repeated DNA component
.
Genome
.
1994
;
37
(
3
):
351
5
.
31.
Marcais
G
,
Kingsford
C
.
A fast, lock-free approach for efficient parallel counting of occurrences of k-mers
.
Bioinformatics
.
2011
;
27
(
6
):
764
70
.
32.
Masumoto
H
,
Nakano
M
,
Ohzeki
J
.
The role of CENP-B and alpha-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres
.
Chromosome Res
.
2004
;
12
(
6
):
543
56
.
33.
Matzke
MA
,
Varga
F
,
Berger
H
,
Schernthaner
J
,
Schweizer
D
,
Mayr
B
,
A 41-42 bp tandemly repeated sequence isolated from nuclear envelopes of chicken erythrocytes is located predominantly on microchromosomes
.
Chromosoma
.
1990
;
99
(
2
):
131
7
.
34.
Matzke
AJ
,
Varga
F
,
Gruendler
P
,
Unfried
I
,
Berger
H
,
Mayr
B
,
Characterization of a new repetitive sequence that is enriched on microchromosomes of turkey
.
Chromosoma
.
1992
;
102
(
1
):
9
14
.
35.
Melters
DP
,
Bradnam
KR
,
Young
HA
,
Telis
N
,
May
MR
,
Ruby
JG
,
Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution
.
Genome Biol
.
2013
;
14
:
R10
.
36.
Muller
H
,
Gil
J
,
Drinnenberg
IA
.
The impact of centromeres on spatial genome architecture
.
Trends Genet
.
2019
;
35
(
8
):
565
78
.
37.
Nishida
C
,
Ishishita
S
,
Yamada
K
,
Griffin
DK
,
Matsuda
Y
.
Dynamic chromosome reorganization in the osprey (Pandion haliaetus, Pandionidae, Falconiformes): relationship between chromosome size and the chromosomal distribution of centromeric repetitive DNA sequences
.
Cytogenet Genome Res
.
2014
;
142
(
3
):
179
89
.
38.
Olsson
U
,
Alström
P
.
A comprehensive phylogeny and taxonomic evaluation of the waxbills (Aves: Estrildidae)
.
Mol Phylogenet Evol
.
2020
;
146
:
106757
.
39.
Pigozzi
MI
,
Solari
AJ
.
Germ cell restriction and regular transmission of an accessory chromosome that mimics a sex body in the zebra finch, Taeniopygia guttata
.
Chromosome Res
.
1998
;
6
(
2
):
105
13
.
40.
Plohl
M
,
Meštrović
N
,
Mravinac
B
.
Centromere identity from the DNA point of view
.
Chromosoma
.
2014
;
123
(
4
):
313
25
.
41.
Rhie
A
,
McCarthy
S
,
Fedrigo
O
,
Damas
J
,
Formenti
G
,
Koren
S
,
Towards complete and error-free genome assemblies of all vertebrate species
.
Nature
.
2021
;
592
:
737
46
.
42.
Romanov
MN
,
Farré
M
,
Lithgow
PE
,
Fowler
KE
,
Skinner
BM
,
O’Connor
R
,
Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
.
BMC Genomics
.
2014
;
15
:
1060
.
43.
Saifitdinova
AF
,
Derjusheva
SE
,
Malykh
AG
,
Zhurov
VG
,
Andreeva
TF
,
Gaginskaya
ER
.
Centromeric tandem repeat from the chaffinch genome: isolation and molecular characterization
.
Genome
.
2001
;
44
(
1
):
96
103
.
44.
Schalch
T
,
Steiner
FA
.
Structure of centromere chromatin: from nucleosome to chromosomal architecture
.
Chromosoma
.
2017
;
126
(
4
):
443
55
.
45.
Shang
WH
,
Hori
T
,
Toyoda
A
,
Kato
J
,
Popendorf
K
,
Sakakibara
Y
,
Chickens possess centromeres with both extended tandem repeats and short non-tandem repetitive sequences
.
Genome Res
.
2010
;
20
(
9
):
1219
28
.
46.
Slate
J
,
Hale
MC
,
Birkhead
TR
.
Simple sequence repeats in zebra finch (Taeniopygia guttata) expressed sequence tags: a new resource for evolutionary genetic studies of passerines
.
BMC Genomics
.
2007
;
8
(
1
):
52
.
47.
Solovei
IV
,
Joffe
BI
,
Gaginskaya
ER
,
Macgregor
HC
.
Transcription of lampbrush chromosomes of a centromerically localized highly repeated DNA in pigeon (Columba) relates to sequence arrangement
.
Chromosome Res
.
1996
;
4
(
8
):
588
603
.
48.
Sumner
AT
.
Chromosomes: organization and function
.
Oxford
:
Blackwell Publishing
;
2003
.
49.
Symonová
R
,
Ocalewicz
K
,
Kirtiklis
L
,
Delmastro
GB
,
Pelikánová
Š
,
Garcia
S
,
Higher-order organisation of extremely amplified, potentially functional and massively methylated 5S rDNA in European pikes (Esox sp.)
.
BMC Genomics
.
2017
;
18
:
391
.
50.
Talbert
PB
,
Henikoff
S
.
What makes a centromere?
Exp Cell Res
.
2020
;
389
(
2
):
111895
.
51.
Tanabe
H
,
Müller
S
,
Neusser
M
,
von Hase
J
,
Calcagno
E
,
Cremer
M
,
Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates
.
Proc Natl Acad Sci U S A
.
2002
;
99
(
7
):
4424
9
.
52.
Tanaka
K
,
Suzuki
T
,
Nojiri
T
,
Yamagata
T
,
Namikawa
T
,
Matsuda
Y
.
Characterization and chromosomal distribution of a novel satellite DNA sequence of Japanese quail (Coturnix coturnix japonica)
.
J Hered
.
2000
;
91
(
5
):
412
5
.
53.
Tanaka
TU
,
Clayton
L
,
Natsume
T
.
Three wise centromere functions: see no error, hear no break, speak no delay
.
EMBO Rep
.
2013
;
14
(
12
):
1073
83
.
54.
Teng
JLL
,
Yeung
ML
,
Chan
E
,
Jia
L
,
Lin
CH
,
Huang
Y
,
PacBio but not Illumina technology can achieve fast, accurate and complete closure of the high GC, complex Burkholderia pseudomallei two-chromosome genome
.
Front Microbiol
.
2017
;
8
:
1448
.
55.
Torgasheva
AA
,
Malinovskaya
LP
,
Zadesenets
KS
,
Karamysheva
TV
,
Kizilova
EA
,
Akberdina
EA
,
Germline-restricted chromosome (GRC) is widespread among songbirds
.
Proc Natl Acad Sci U S A
.
2019
;
116
(
24
):
11845
50
.
56.
Uno
Y
,
Nishida
C
,
Hata
A
,
Ishishita
S
,
Matsuda
Y
.
Molecular cytogenetic characterization of repetitive sequences comprising centromeric heterochromatin in three Anseriformes species
.
PLoS One
.
2019
;
14
(
3
):
e0214028
.
57.
Van Hooser
AA
,
Ouspenski
II
,
Gregson
HC
,
Starr
DA
,
Yen
TJ
,
Goldberg
ML
,
Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A
.
J Cell Sci
.
2001
;
114
(
Pt 19
):
3529
42
.
58.
Warren
WC
,
Clayton
DF
,
Ellegren
H
,
Arnold
AP
,
Hillier
LW
,
Kunstner
A
,
The genome of a songbird
.
Nature
.
2010
;
464
(
7289
):
757
62
.
59.
Waye
JS
,
Durfy
SJ
,
Pinkel
D
,
Kenwrick
S
,
Patterson
M
,
Davies
KE
,
Chromosome-specific alpha satellite DNA from human chromosome 1: hierarchical structure and genomic organization of a polymorphic domain spanning several hundred kilobase pairs of centromeric DNA
.
Genomics
.
1987
;
1
(
1
):
43
51
.
60.
Yamada
K
,
Shibusawa
M
,
Tsudzuki
M
,
Matsuda
Y
.
Molecular cloning and characterization of novel centromeric repetitive DNA sequences in the blue-breasted quail (Coturnix chinensis, Galliformes)
.
Cytogenet Genome Res
.
2002
;
98
(
4
):
255
61
.
61.
Yamada
K
,
Nishida-Umehara
C
,
Matsuda
Y
.
A new family of satellite DNA sequences as a major component of centromeric heterochromatin in owls (Strigiformes)
.
Chromosoma
.
2004
;
112
(
6
):
277
87
.
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