Abstract
Introduction: The mapping of the satellite DNA on chromosomes is vital to understanding the distribution and evolution of repetitions in the genome since these chromosomal studies have shown the origin, evolutionary mode, and function of repetitive sequences. This study aimed to prospect the satellitome and determine its location in the genome of two cryptic species of Hypostomus, H. aff. ancistroides and H. ancistroides, with and without XX/XY sexual chromosome system. Methods: Mitotic chromosomes and DNA extraction were obtained according to protocols. After the whole genome sequencing, the satDNAs were retrieved, amplified, and hybridized in chromosome preparations for male and female individuals. Results: We found 30 satellite families (47 variants, two superfamilies) in H. ancistroides and 38 satellite families (45 variants, four superfamilies) in H. aff. ancistroides. The sequences varied from 14 bp to 2,662 bp in H. ancistroides and from 14 bp to 2,918 bp in H. aff. ancistroides. We did not observe any tandem repeats that were exclusive to each of the libraries; however, many sequences showed very different abundances and copy numbers between the libraries. Four satDNAs did not hybridize on the chromosomes of either species. Conversely, one satDNA hybridized in both species, HxySat1-80. However, the phenotypes found varied among species, populations, and in the same individual. There was no sign of HanSat3-464 and HanSat11-335 in any individuals of H. aff. ancistroides, but markings were in the chromosomes of H. ancistroides. HxySat12-1127 and HxySat8-52, on the other hand, were only hybridized in H. aff. ancistroides, while H. ancistroides had a negative sign. No hybridization of satDNAs was found in the X and Y sex chromosomes as they were mostly composed of euchromatin. Conclusion: We distinguish H. aff. ancistroides as genetically different from H. ancistroides, recognizing that such characteristics go far beyond morphological, karyotypic, and molecular data. Our data support the differential abundance and location of satellite DNAs and confirm that many organisms, including fish, have repetitive sequences that validate the library hypothesis. All found and validated satDNAs and the characterization of the satellitomes of the two species represent important contributions to cytogenomic studies of the genus Hypostomus.
Journal Section:
Research Article
References
1.
Britski
HA
. Peixes de água doce do Estado de São Paulo: Sistemática
. In: Piscicultura Pe, editor. Faculdade de Saúde Pública da Universidade de São Paulo: Instituto de Pesca da Coordenadoria da Pesquisa de Recursos Naturais da Secretaria da Agricultura
; 1972
. p. 79
–108
.2.
Rocha-Reis
DA
, Pasa
R
, Kavalco
KF
. High congruence of karyotypic and molecular data on Hypostomus species from Brazilian southeast
. Org Divers Evol
. 2021
;21
(1
):135
–43
. 3.
Hollanda Carvalho
PH
. Análises filogenéticas e filogeográficas do complexo de espécies Hypostomus ancistroides (Siluriformes: Loricariidae)
. Thesis
: Universidade de São Paulo
; 2011
.4.
Artoni
RF
, Bertollo
LAC
. Cytogenetic studies on Hypostominae (pisces, Siluriformes, Loricariidae). Considerations on karyotype evolution in the genus Hypostomus
. Caryologia
. 1996
;49
(1
):81
–90
. 5.
Alves
AL
, Oliveira
C
, Nirchio
M
, Granado
A
, Foresti
F
. Karyotypic relationships among the tribes of Hypostominae (Siluriformes: Loricariidae) with description of XO sex chromosome system in a Neotropical fish species
. Genetica
. 2006
;128
(1–3
):1
–9
. 6.
Alves
AL
, de Borba
RS
, Pozzobon
APB
, Oliveira
C
, Nirchio
M
, Granado
A
, et al. Localization of 18S ribosomal genes in suckermouth armoured catfishes Loricariidae (Teleostei, Siluriformes) with discussion on the Ag-NOR evolution
. Comp Cytogenet
. 2012
;6
(3
):315
–21
. 7.
Rubert
M
, da Rosa
R
, Jerep
FC
, Bertollo
LAC
, Giuliano Caetano
L
. Cytogenetic characterization of four species of the genus Hypostomus Lacépède
. Comp Cytogenet
. 2011
;5
:397
–410
. 8.
Bueno
V
, Zawadzki
CH
, Margarido
VP
. Trends in chromosome evolution in the genus Hypostomus Lacépède, 1803 (Osteichthyes, Loricariidae): a new perspective about the correlation between diploid number and chromosomes types
. Rev Fish Biol Fish
. 2012
;22
(1
):241
–50
. 9.
Endo
KS
, Martinez
ERM
, Zawadzki
CH
, Paiva
LRDS
, Júlio Júnior
HF
. Karyotype description of possible new species of the Hypostomus ancistroides complex (Teleostei: Loricariidae) and other Hypostominae
. Acta Sci Biol Sci
. 2012
;34
(2
):181
–9
. 10.
Fernandes
CA
, Damásio
JF
, Martins-Santos
IC
. Cytogenetic studies in species of family Loricariidae (Osteichthyes, Siluriformes) from Iguatemi river basin, Brazil. First cytogenetic report in Farlowella amazonum (Günther, 1864)
. Caryologia
. 2012
;65
(4
):276
–80
. 11.
Maurutto
FAM
, Manvailer
LFS
, Sczepanski
TS
, Cestari
MM
, Artoni
RF
. Cytogenetic characterization of three allopatric species of Hypostomus Lacépède (1803) (Teleostei, Loricariidae)
. Caryologia
. 2012
;65
(4
):340
–6
. 12.
Pansonato-Alves
JC
, Serrano
EA
, Utsunomia
R
, Scacchetti
PC
, Oliveira
C
, Foresti
F
. Mapping five repetitive DNA classes in sympatric species of Hypostomus (Teleostei: Siluriformes: Loricariidae): analysis of chromosomal variability
. Rev Fish Biol Fish
. 2013
;23
(4
):477
–89
. 13.
Traldi
JB
, Blanco
DR
, Vicari
MR
, Martinez
JF
, Lui
RL
, Barros
AV
, et al. Chromosomal diversity in Hypostomus (Siluriformes, Loricariidae) with emphasis on physical mapping of 18S and 5S rDNA sites
. Genet Mol Res
. 2013
;12
(1
):463
–71
. 14.
Lara Kamei
MCS
, Baumgärtner
L
, Paiva
S
, Zawadzki
CH
, Martins-Santos
IC
, Portela-Castro
ALDB
. Chromosomal diversity of three species of Hypostomus Lacépède, 1803 (Siluriformes, Loricariidae), from the Paraná River Basin, Brazil: a species complex in Hypostomus ancistroides reinforced by a ZZ/ZW sex chromosome system
. Zebrafish
. 2017
;14
(4
):357
–63
. 15.
Rocha-Reis
DA
, de Oliveira Brandão
K
, de Almeida-Toledo
LF
, Pazza
R
, Kavalco
KF
. The persevering cytotaxonomy: discovery of a unique XX/XY sex chromosome system in catfishes suggests the existence of a new, endemic and rare species
. Cytogenet Genome Res
. 2018
;156
(1
):45
–55
. 16.
John
B
, Miklos
GL
. Functional aspects of satellite DNA and heterochromatin
. Int Rev Cytol
. 1979
;58
:1
–114
. 17.
Choo
KH
, Vissel
B
, Earle
E
. Evolution of alpha-satellite DNA on human acrocentric chromosomes
. Genomics
. 1989
;5
(2
):332
–44
. 18.
Charlesworth
B
, Sniegowski
P
, Stephan
W
. The evolutionary dynamics of repetitive DNA in eukaryotes
. Nature
. 1994
;371
(6494
):215
–20
. 19.
Jurka
J
, Kapitonov
VV
, Pavlicek
A
, Klonowski
P
, Kohany
O
, Walichiewicz
J
. Repbase update, a database of eukaryotic repetitive elements
. Cytogenet Genome Res
. 2005
;110
(1–4
):462
–7
. 20.
Camacho
JPM
, Ruiz-Ruano
FJ
, Martín-Blázquez
R
, López-León
MD
, Cabrero
J
, Lorite
P
, et al. A step to the gigantic genome of the desert locust: chromosome sizes and repeated DNAs
. Chromosoma
. 2015
;124
(2
):263
–75
. 21.
Novák
P
, Neumann
P
, Macas
J
. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data
. BMC Bioinform
. 2010
;11
:378
. 22.
Novák
P
, Neumann
P
, Pech
J
, Steinhaisl
J
, Macas
J
. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads
. Bioinformatics
. 2013
;29
(6
):792
–3
. 23.
Biscotti
MA
, Olmo
E
, Heslop-Harrison
JSP
. Repetitive DNA in eukaryotic genomes
. Chromosome Res
. 2015
;23
(3
):415
–20
. 24.
Gold
JR
, Li
C
, Shipley
N
, Powers
PK
. Improved methods for working with fish chromosomes with a review of metaphase chromosome banding
. J Fish Biol
. 1990
;37
(4
):563
–75
. 25.
Afgan
E
, Baker
D
, Batut
B
, van den Beek
M
, Bouvier
D
, Cech
M
, et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update
. Nucleic Acids Res
. 2018
;46
(W1
):W537
–44
. 26.
Andrews
S
. FastQC: a quality control tool for high throughput sequence data
. 2010
. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc27.
Bolger
AM
, Lohse
M
, Usadel
B
. Trimmomatic: a flexible trimmer for Illumina sequence data
. Bioinformatics
. 2014
;30
(15
):2114
–20
. 28.
Novák
P
, Ávila Robledillo
L
, Koblízková
A
, Vrbová
I
, Neumann
P
, Macas
J
. TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads
. Nucleic Acids Res
. 2017
;45
(12
):e111
. 29.
Langmead
B
, Salzberg
SL
. Fast gapped-read alignment with Bowtie 2
. Nat Methods
. 2012
;9
(4
):357
–9
. 30.
Ruiz-Ruano
FJ
, López-León
MD
, Cabrero
J
, Camacho
JPM
. High-throughput analysis of the satellitome illuminates satellite DNA evolution
. Sci Rep
. 2016
;6
:28333
. 31.
Okonechnikov
K
, Conesa
A
, García-Alcalde
F
. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data
. Bioinfoamtics
. 2016
;32
(2
):292
–4
. 32.
Tamura
K
, Stecher
G
, Kumar
S
. MEGA11: molecular evolutionary Genetics analysis version 11
. Mol Biol Evol
. 2021
;38
(7
):3022
–7
. 33.
Li
W
, Godzik
A
. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences
. Bioinformatics
. 2006
;22
(13
):1658
–9
. 34.
Schwarzacher
T
, Heslop-Harrison
P
. Practical in situ hybridization
. Oxford
: BIOS Scientific Publishers
; 2000
.35.
Schneider
CA
, Rasband
WS
, Eliceiri
KW
. NIH Image to IMAGEJ: 25 years of image analysis
. Nat Methods
. 2012
;9
(7
):671
–5
. 36.
Jiang
Y
, Gao
X
, Liu
S
, Zhang
Y
, Liu
H
, Sun
F
, et al. Whole genome comparative analysis of channel catfish (Ictalurus punctatus) with four model fish species
. BMC Genomics
. 2013
;14
:780
. 37.
Santos
GED
. Análises citogenômicas comparativas em Ancistrus (Siluriformes: Loricariidae)
. Dissertation
: Universidade Estadual Paulista
; 2022
.38.
Oliveira
JVL
. Descrição de uma nova variante cariotípica e caracterização do mitogenoma e satelitoma de Rineloricaria lanceolata (Siluriformes, Loricariidae)
. Universidade Estadual do Centro-Oeste do Paraná
; 2022
. Dissertation.39.
Rocha-Reis
DA
, Kavalco
KF
, de Oliveira Brandão
K
, Dergam
JA
, Pasa
R
. Evolutionary trends in species complex diagnosed by cytogenetic polymorphism: the case of Hypostomus ancistroides (Siluriformes, Loricariidae)
. bioRxiv
; 2020
. 40.
Taboada
X
, Rey
M
, Bouza
C
, Viñas
A
. Cytogenomic analysis of several repetitive DNA elements in turbot (Scophthalmus maximus)
. Gene
. 2018
;644
:4
–12
. 41.
Fry
K
, Salser
W
. Nucleotide sequences of HS-alpha satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents
. Cell
. 1977
;12
(4
):1069
–84
. 42.
Plohl
M
, Meštrovic
N
, Mravinac
B
. Satellite DNA evolution
. In: Garrido-Ramos
MA
, editor. Repetitive DNA
. Basel
: Karger
; 2012
. p. 126
–52
.43.
Utsunomia
R
, Ruiz-Ruano
FJ
, Silva
DMZA
, Serrano
EA
, Rosa
IF
, Scudeler
PES
, et al. A glimpse into the satellite DNA library in Characidae fish (Teleostei, Characiformes)
. Front Genet
. 2017
;8
:103
. 44.
Long
EO
, Dawid
IB
. Repeated genes in eukaryotes
. Annu Rev Biochem
. 1980
;49
:727
–64
. 45.
Singer
MF
. Highly repeated sequences in mammalian genomes
. Int Rev Cytol
. 1982
;76
:67
–112
. 46.
Southern
EM
. DNA sequences and chromosome structure
. J Cell Sci Suppl
. 1984
;1
:31
–41
. 47.
Cioffi
MB
, Moreira-Filho
O
, Almeida-Toledo
LF
, Bertollo
LAC
. The contrasting role of heterochromatin in the differentiation of sex chromosomes: an overview from Neotropical fishes
. J Fish Biol
. 2012
;80
(6
):2125
–39
. 48.
Macas
J
, Kejnovský
E
, Neumann
P
, Novák
P
, Koblížková
A
, Vyskot
B
. Next generation sequencing-based analysis of repetitive DNA in the model dioecious plant Silene latifolia
. PLoS One
. 2011
;6
(11
):e27335
. 49.
Hobza
R
, Lengerova
M
, Svoboda
J
, Kubekova
H
, Kejnovsky
E
, Vyskot
B
. An accumulation of tandem DNA repeats on the Y chromosome in Silene latifolia during early stages of sex chromosome evolution
. Chromosoma
. 2006
;115
(5
):376
–82
. 50.
Kubat
Z
, Hobza
R
, Vyskot
B
, Kejnovsky
E
. Microsatellite accumulation on the Y chromosome in Silene latifolia
. Genome
. 2008
;51
(5
):350
–6
. 51.
Rocha-Reis
DA
, Pasa
R
, Menegidio
FB
, Heslop-Harrison
JS
, Schwarzacher
T
, Kavalco
KF
. The complete mitochondrial genome of two armored catfish populations of the genus Hypostomus (Siluriformes, Loricariidae, Hypostominae)
. Front Ecol Evol
. 2020
;8
. 52.
Garrido-Ramos
MA
, de la Herrán
R
, Jamilena
M
, Lozano
R
, Ruiz Rejón
C
, Ruiz Rejón
M
. Evolution of centromeric satellite DNA and its use in phylogenetic studies of the Sparidae family (Pisces, Perciformes)
. Mol Phylogenet Evol
. 1999
;12
(2
):200
–4
. 53.
Leclerc
GM
, Han
K
, Leclerc
GJ
, Ely
B
. Characterization of a highly repetitive sequence conserved among the North American Morone species
. Mar Biotechnol
. 1999
;1
(2
):122
–30
. 54.
de la Herrán
R
, Rejon
CR
, Rejon
MR
, Garrido-Ramos
MA
. The molecular phylogeny of the Sparidae (Pisces, Perciformes) based on two satellite DNA families
. Heredity
. 2001
;87
(Pt 6
):691
–7
. 55.
Lanfredi
M
, Congiu
L
, Garrido-Ramos
MA
, de la Herrán
R
, Leis
M
, Chicca
M
, et al. Chromosomal location and evolution of a satellite DNA family in seven sturgeon species
. Chromosome Res
. 2001
;9
(1
):47
–52
. 56.
Robles
F
, de la Herrán
R
, Ludwig
A
, Ruiz Rejón
C
, Ruiz Rejón
M
, Garrido-Ramos
MA
. Evolution of ancient satellite DNAs in sturgeon genomes
. Gene
. 2004
;338
(1
):133
–42
. 57.
Martins
C
, Ferreira
IA
, Oliveira
C
, Foresti
F
, Galetti
PM
Jr. A tandemly repetitive centromeric DNA sequence of the fish Hoplias malabaricus (Characiformes: erythrinidae) is derived from 5S rDNA
. Genetica
. 2006
;127
(1–3
):133
–41
. 58.
Silva
DMZA
, Utsunomia
R
, Ruiz-Ruano
FJ
, Daniel
SN
, Porto-Foresti
F
, Hashimoto
DT
, et al. High-throughput analysis unveils a highly shared satellite DNA library among three species of fish genus Astyanax
. Sci Rep
. 2017
;7
(1
):12726
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