ANIMAL GENETICS ORIGINAL PAPER

Screening of SSR markers associated with scale cover

pattern and mapped to a genetic linkage map of common carp
(Cyprinus carpio L.)
Tongqian Xiao & Cuiyun Lu & Yulan Xu & Chao Li &
Xianhu Zheng & Dingchen Cao & Lei Cheng &
Shahid Mahboob & Xiaowen Sun
Received: 23 May 2014 / Revised: 30 September 2014 / Accepted: 1 October 2014
#Institute of Plant Genetics, Polish Academy of Sciences, Poznan 2014
Abstract Fish scale is an attractive model in bone physiology
research and is also a crucial character for breeding new
varieties. Thus, it is important to identify loci in the genome
associated with scale formation. In this study, 290 microsat-
ellite markers in common carp (Cyprinus carpio L.) were
selected and tested for their segregation in a full-sib mapping
panel containing 96 individuals (population 1). Association
analysis identified seven simple sequence repeats (SSRs)
(HLJ2509, HLJ3227, HLJ3675, HLJ3766, HLJ3863, FGFR1,
FGFR7) that showed significant correlation with scale cover
pattern in population 1. When the seven SSRs were investi-
gated in two other populations, seven and five SSRs were
significantly correlated with scale cover pattern in population
2 (116 individuals) and population 3 (57 individuals), respec-
tively. The exceptions were FGFR1 and HLJ3227. A genetic
linkage map was constructed using the 290 SSRs and 241
SSRs were mapped into 47 linkage groups (LGs), with 215
markers per LG. The map spanned 2,241.7 cM, with LG sizes
that varied from1.1 to 124.9 cM. All seven markers associated
with scale cover mapped into LG3. We considered that a gene
cluster that affected the scale cover pattern possibly existed in
LG3. By aligning the seven markers with the zebrafish (Danio
rerio) genome, we identified six candidate genes (atoh1a,
ptch1, bmp1a, fgfr1a, fgf17, wnt5a) that may be associated
with scale formation. We propose that the seven markers could
be used with marker-assisted selection to breed a new variety
of common carp, and the six candidate genes could help in
understanding the scale cover mechanism.
Keywords Common carp
.
Linkage map
.
Microsatellite
markers
.
Scale cover pattern
Introduction
Fish scales are protective and are a traditionally used pheno-
type. Based on the morphology, the scale cover process has
been described in numerous species, such as White crappie
(Pomoxis annularis), Atlantic croaker (Micropogon
undulatus), and Spotted sucker (Minytrema melanops) (Siefert
1965; Bridges 1971; White 1977). The structure of a single
zebrafish (Danio rerio) scale and the participation of various
cell types (e.g., osteoblast and osteoclast) in scale formation
have been reported (Metz et al. 2012). Interestingly, the scale
exhibits many structural and physiological characteristics that
are similar to mammalian bone, especially the elasmoid scale
(De Vrieze et al. 2010; Yoshikubo et al. 2005). Moreover,
scales possess many advantageous characteristics; e.g., they
can be used both in vivo and in vitro, they are easily harvested,
they carry bone-degrading and bone-forming cell populations,
and the scales regenerate (Metz et al. 2012). As a result,
elasmoid scales are considered as an attractive model for bone
physiology research in mammals. Thus, an understanding of
Tongqian Xiao and Cuiyun Lu contributed equally to this work.
T. Xiao
:
C. Lu
:
Y. Xu
:
C. Li
:
X. Zheng
:
D. Cao
:
L. Cheng
:
X. Sun (*)
Heilongjiang Fisheries Research Institute, Chinese Academy of
Fisheries Sciences, No. 232 Hesong Road, Daoli District,
Harbin 150070, Heilongjiang, China
e-mail: sunxw2002@163.com
T. Xiao
College of Fisheries and Life Science, Dalian Ocean University,
District Shahekou, Dalian 116023, China
C. Lu
Alkali Soil Natural Environmental Science Center, Northeast
Forestry University, Harbin 150040, China
S. Mahboob
Department of Zoology, College of Science, King Saud University,
Riyadh 11451, Saudi Arabia
J Appl Genetics
DOI 10.1007/s13353-014-0250-9
the molecular mechanismof scale formation may contribute to
the development of new therapeutic methods for skeletal
diseases.
Rudzinskie (1928) reported that the complete scale cover in
the common carp showed dominance over the mirror carp. In
subsequent studies (Kirpitchnikov and Balkashina 1935,
1936; Kirpitchnikov 1937, 1999), it was presumed that two
independent loci (S, N) in common carp were responsible for
the pattern of scale cover: the S mutation generated a scattered
scale pattern and the N mutation caused a linear scale pattern.
Even in a scattered scale pattern, the distribution of the scale
patterns is various, which strongly supports the existence of
numerous modifier genes. To date, the genes represented by
the S and N loci are unknown. Nevertheless, in recent years,
many of the genes involved in the control of scale formation
have been identified; for example, ectodysplasin A (eda),
ectodysplasin A receptor (edar) mutants (Harris et al. 2008),
fibroblast growth factor receptor 1 (fgfr1) (Rohner et al. 2009),
and adenine nucleotide translocators (ant). Despite this, the
molecular mechanism used in the scale cover process is still
not understood. Thus, identifying other genes related to scale
forming is still a crucial objective.
Fish scales are bony structures that grow shingle-like from
pockets within the skin (Schneider et al. 2000). Recently, the
scales of fishes were explored for age determination and
growth history (Fisher and Pearcy 2005). The daily circulus
deposition on fish scales was shown to be a feasible means of
estimating daily growth and growth impairment (Cheung et al.
2007). Thus, the phenotypic character of fish scale is a worthy
of further study.
Scale could serve as a phenotypic target for selection
during domestication. A stable genetic performance is essen-
tial for new varieties; therefore, in systemic breeding or cross-
breeding, the required properties and other phenotypic char-
acters should be fixed. Generally, inbreeding or backcross
breeding methods require several generations in order to select
the required characters. Marker-assisted selection (MAS) and
marker-assisted gene introgression (MAI) can shorten the
selection time significantly (Sun 2010). Identifying molecular
markers or genes linked with characters of interest is the first
step, and it is necessary to construct a genetic linkage map
based on molecular markers. Because of the widespread in-
terest in molecular breeding in common carp, many polymor-
phic markers have been developed (David et al. 2001) and a
genetic linkage map of common carp has been constructed
with microsatellites and randomamplification of polymorphic
DNA (RAPD) markers by Sun and Liang (2004). Zhang et al.
(2011) analyzed muscle fiber-related quantitative trait loci
(QTL) in common carp, Xu et al. (2013) studied a QTL related
to superoxide dismutase in mirror carp, and Wang et al. (2012)
mapped the QTL of growth-related traits in common carp.
However, no studies on fish scale have been reported so far. In
this study, microsatellite markers associated with scale were
screened and a genetic map based on these markers was
constructed.
In this study, 260 microsatellite markers in common carp
(Cyprinus carpio L.) were chosen among the microsatellite
markers developed at the Heilongjiang Fisheries Research
Institute (Harbin, China). In addition, 30 microsatellite
markers were selected from homologous sequences in the
common carp genome of the ant, eda, edar, and fgfr genes
that have been shown to be associated with scale formation in
common carp or zebrafish. A genetic linkage map was con-
structed and a comparative analysis of the significant
correlation markers against the zebrafish genome was
conducted to identify genes that might control scale
cover patterns in common carp.
Materials and methods
Fish material and evaluation of phenotypic trait
Three populations of common carp were investigated in this
study; one population was used as the mapping and screening
population, and the other two were the validation groups.
A cross between Amur wild carp (Cyprinus carpio
haematopterus) and Mirror carp (Cyprinus carpio L.) was
performed at the Song Pu Aquaculture Experimental Station
(Harbin, China) in spring 2007, forming a full-sib family with
the same scale phenotype (the complete scale cover pattern).
Subsequently, 75 polymorphic microsatellites were genotyped
in the F1 individuals. Genetic distances among individuals
were estimated using genetic similarity according to Nei and
Li (1979). Crosses were performed by selecting one male
female pair. The offspring conformed to the Mendelian phe-
notype separation. We chose 55 individuals with missing scale
and 41 individuals with full scales. These 96 progenies from
the full-sib family and their parents (population 1) were used
to develop the linkage map.
In the same way, another cross between German mirror
carp and Amur wild carp was performed in 2009. Three
mature F1 individuals (one female and two males) were
selected to produce two full-sib families. After rearing for
6 months, a total of 116 (population 2) and 57 (population
3) individuals were collected from the two full-sib families as
the validation groups.
The scale trait was scored according to the covered level as
follows: class 0=individuals with missing scale, class 1=
individuals with full scale.
DNA extraction and microsatellite genotyping
Genomic DNAwas isolated from fin clips according to stan-
dard phenol-chloroform protocol. The concentration and
J Appl Genetics
quality of the purified DNAwere tested using spectrophotom-
etry and verified by agarose gel electrophoresis.
From the microsatellite markers developed at the Heilong-
jiang Fisheries Research Institute, 260 microsatellite markers
were chosen for the genome scan. An additional 30 simple
sequence repeats (SSRs) that were derived from the ant, eda,
edar, and fgfr gene sequences and their context in common
carp were included to give the 290 microsatellite markers that
were used in this study. The microsatellite primers were de-
signed using Primer3 (http://primer3.ut.ee/).
Polymerase chain reaction (PCR) assays were performed in
an 11-L mixture containing 1PCR buffer with 2 mM
MgCl
2
, 1U Taq DNA polymerase, 125 M each dNTP,
5 M each primer, and 50 ng genomic DNA. PCR amplifica-
tions were carried out as follows: initial denaturation at 94 C
for 5 min, followed by 27 cycles of denaturation at 94 C for
Table 1 Association analysis between simple sequence repeat (SSR) markers and scale cover patterns and the genotype distribution of each marker in
three populations. The Chi-squared test results are shown
Markers Population 1 Population 2 Population 3
Genotype N
0
N
1
P Genotype N
0
N
1
P Genotype N
0
N
1
P
FGFR1 4.56E13
b
2.62E4
a
3.71E3
AA 53 8 AB 26 57 AB 13 25
AB 2 13 BB 0 33 BB 0 19
BB 0 19
FGFR7 1.02E15
b
6.47E26
b
1.63E4
a
AA 55 9 AA 0 32 AB 0 17
AB 0 32 AB 0 58 AC 0 11
BB 26 0 BC 0 16
CC 13 0
HLJ2509 2.21E10
b
5.47E16
b
1.36E6
b
AB 7 14 AA 0 30 AB 0 11
AC 0 12 AB 5 56 AC 0 17
BB 43 4 BB 21 4 BD 9 2
BC 5 11 CD 4 14
HLJ3227 2.07E13
b
8.01E4
a
1.16E2
AB 2 31 AA 12 17 AB 6 9
BB 53 10 AB 13 38 AC 6 7
BB 1 35 BD 1 13
CD 0 13
HLJ3675 6.11E5
a
1.68E12
b
4.32E4
a
AA 51 24 AA 19 6 AB 11 8
AB 4 17 AB 7 53 AD 1 15
BB 0 31 BC 1 8
CD 0 12
HLJ3766 1.08E16
b
2.94E11
b
2.04E5
b
AA 52 2 AA 21 11 AC 11 6
AB 2 12 AB 5 47 AD 1 10
AC 1 9 BB 0 32 BC 1 17
BC 0 18 BD 0 11
HLJ3863 3.30E18
b
3.33E21
b
9.89E5
a
AB 1 13 AA 0 35 AB 0 27
AC 0 18 AB 2 53 BB 13 17
BB 53 1 BB 24 2
BC 1 9
a
Marker was significantly correlated with scale cover pattern after Bonferroni correction (adjusted P-value=8.72E4)
b
Marker was extremely significantly correlated with scale cover pattern after Bonferroni correction (adjusted P-value=3.45E5)
N
0
, missing scale pattern genotype; N
1
, full scale pattern genotype
J Appl Genetics
30 s, annealing for 30 s, and extension at 72 C for 30 s, and a
final extension at 72 C for 5 min. The amplified products
were separated on 8 % polyacrylamide gel electrophoresis
(PAGE) gels and visualized using silver staining. The product
size was determined by comparison with the standard marker
using Gel-Pro32.
Association analysis in the three populations
An association analysis between microsatellite markers and
the pattern of scale cover in population 1 was conducted using
SPSS version 17.0 (Chicago, IL, USA). Because the pheno-
type data of scale cover pattern was a categorical variable, the
association for each marker was subjected to a Chi-squared
test in crosstabs (Galli et al. 2010). The significance level was
set at P<0.05. All the results were corrected using the
Bonferroni correction.
In the same way, an association analysis of the significant
correlated markers that were obtained from the association
analysis in population 1 was performed to verify their reliabil-
ity in population 2 and population 3.
Construction of a genetic linkage map of common carp
Alinkage map based on the 290 microsatellites was construct-
ed using JoinMap 4.0 (Van Ooijen 2006). A Chi-squared test
was performed to detect the segregation distortion at each
marker locus. An LOD score >3 was considered to establish
significant linkage. Adjacent triplets were repeatedly tested to
optimize the marker order.
The genome length based on the linkage map was estimat-
ed by two different methods: Ge1, where terminal chromo-
some regions were considered by adding two times the aver-
age spacing of markers (Fishman et al. 2001), and Ge2, where
the observed lengths of the linkage groups multiplied by factor
(m+1)/(m1) were considered and m is the number of loci in
each group (Zheng et al. 2011). The average of these two
values was considered as the estimated genome size.
Mapping the markers to the zebrafish genome
Markers associated with scale cover were mapped to the
zebrafish genome to determine the location of these markers
in the zebrafish genome. NCBI BLASTNwas used with a cut-
off E-value of <e
5
to find syntenic regions in the zebrafish
genomes. The syntenic regions and their context were scanned
to find candidate genes likely associated with the scale cover
patterns, based on previously published studies.
Results
Microsatellite genotyping
All 290 microsatellite markers selected in this study were
successfully amplified by PCR. The markers were found to
be polymorphic in population 1. All 290 markers were used in
the association analysis. Fourteen of the markers were deleted
from the analysis because they showed a significant level of
distorted segregation in the Chi-squared test. Thus, 276 mi-
crosatellite markers were used in the linkage mapping
analysis.
Association analysis in the three populations
An association analysis between the SSRs and the scale
cover pattern was conducted using the Chi-squared test in
crosstabs. Seven SSRs showed significant correlation with
scale cover pattern in population 1. Among them, five
markers (HLJ2509, HLJ3227, HLJ3675, HLJ3766,
HLJ3863) were from markers developed at the Heilong-
jiang Fisheries Research Institute and two (FGFR1,
FGFR7) were derived from the fgfr1a gene in common
carp. The genotype distribution of each marker in the
population is listed in Table 1, and the electrophoretogram
of FGFR7 in population 1 is shown in Fig. 1. The corrected
verification results (Table 1) in the validation populations
Fig. 1 Polyacrylamide gel electrophoresis (PAGE) of FGFR7 in population 1. Numbers 155 are the missing scale individuals and numbers 5696 are
the full-scale individuals
J Appl Genetics
Fig. 2 Genetic linkage map of common carp based on 241 simple sequence repeats (SSRs)
J Appl Genetics
show that the seven SSRs in population 2 and five SSRs in
population 3 were significantly correlated with the scale
cover pattern (P<0.01). The exceptions in population 3
were FGFR1 and HLJ3227. Thus, among the 21 P-values
for the correlations, 19 (90 %) were significant and the five
common markers showed significant correlations in all
three populations.
Linkage map
We constructed a linkage map for common carp with the 276
microsatellite markers. Thirty-five of the markers had LOD
scores below 3.0 and could not be mapped. The remaining
241 microsatellite markers fell into 47 linkage groups (LGs),
with 215 markers per LG (Fig. 2). The linkage map spanned
Fig. 2 continued.
J Appl Genetics
a recombination distance of 2,241.7 cM, with LG sizes that
varied from 1.1 to 124.9 cM. The average mapped distance
between the markers was 11.56 cM. The two map lengths
were estimated as 3,327.88 cM(Ge1) and 3,554.07 cM(Ge2),
giving an average map length of 3,440.95 cM and a genome
coverage rate of 65.15 %. The 241 mapped markers were
consistent with the 212 markers developed at the Heilongjiang
Fisheries Research Institute and 29 markers derived from the
ant, eda, edar, and fgfr sequences and their context in com-
mon carp. Markers derived from ant were mapped into three
LGs (LG1, LG7, LG12), those from eda were mapped into
two LGs (LG11, LG12), those from edar were mapped into
two LGs (LG25, LG30), and those from fgfr were mapped
into four LGs (LG3, LG20, LG31, LG45).
Identifying candidate genes for scale cover pattern
The seven markers that were associated with scale cover
pattern were compared against the zebrafish genome using
BLAST searches. Six markers (HLJ3863, FGFR1, FGFR7,
HLJ3766, HLJ2509, HLJ3675) shared high homology (E-
value<e
5
) with the zebrafish sequence; five of these markers
(FGFR1, FGFR7, HLJ3766, HLJ2509, HLJ3675) were in
syntenic regions in chromosome 8 of zebrafish (Table 2).
Based on the syntenic regions in the zebrafish genome, the
3032-Mb, 3435-Mb, and 5356-Mb regions of chromosome
8 were scanned to identify candidate genes that may be asso-
ciated with scale formation. Based on previous studies and on
our results, we identified six candidate genes (atoh1a, ptch1,
bmp1a, fgfr1a, fgf17, and wnt5a). Their locations, functions,
and predicted signaling pathways are listed in Table 3.
Discussion
Mapping of loci associated with scale cover pattern
The 241 mapped microsatellite markers fell into 47 LGs in the
linkage map of common carp constructed in this study. This
number of LGs is lower than in previous studies. For example,
Sun and Liang (2004) reported 50 LGs, Zhang et al. (2011)
54, and Zheng et al. (2011) 50. The smaller scale of markers
used for the mapping may possibly not be enough for covering
the genome, and that may contribute to the lower LGs number.
In this study, the parents of the mapping population were one
malefemale pair in F1, the closer genetic relationship may
lead to the partial chromosome missing identification, espe-
cially for the smaller scale of samples and markers.
Table 3 Location, function, and signaling pathway of six candidate genes likely associated with scale formation in common carp
Gene name Location in zebrafish Function Signaling pathway Reference
atoh1a Chromosome 8 3044205030442926 Affects morphogenesis of the posterior
lateral line primordium in zebrafish
Wnt-dependent
FGF
Matsuda and Chitnis
(2010)
ptch1 Chromosome 8 3081068430916319 Promotes perichondral osteoblast differentiation
during vertebrate skeletal development
Hedgehog Felber et al. (2011)
bmp1a Chromosome 8 5345543353571312 Affects bone formation and stability BMP/BMPR Asharani et al. (2012)
fgfr1a Chromosome 8 5371260853785291 Affects scale formation FGF/FGFR Rohner et al. (2009)
fgf17 Chromosome 8 5494620854959526 Helps patterning zebrafish embryos FGF/FGFR Cao et al. (2004)
wnt5a Chromosome 8 5591704755926770 Acts as a chemoattractant in the emerging
limb bud, where it contributes to the
establishment of cell polarity that is likely
to underlie the oriented cell behaviors
Wnt Wyngaarden et al.
(2010)
Table 2 NCBI BLAST results for the seven markers associated with scale cover pattern
Linkage group Locus in linkage
group (cM)
Marker Accession no. Zebrafish
chromosome
E-value Region in zebrafish
chromosome (Mb)
3 0 HLJ3863 JQ390340 4 3.00E
26
38.1555
18.0 FGFR1 KJ434008 8 9.00E
43
53.7853
25.7 FGFR7 KJ434009 8 4.00E
56
53.7177
30.5 HLJ3227 JQ390339
31.8 HLJ3766 JN687093 8 7.00E
79
34.7139
47.9 HLJ2509 JQ390338 8 2.00E
6
55.6832
53.7 HLJ3675 JN687071 8 2.00E
15
31.3265
J Appl Genetics
The seven markers associated with scale cover pattern all
mapped into LG3. The FGFR1 and FGFR7 markers were
derived from fgfr1a, implying that fgfr1a may also be located
in LG3. Previous researches have suggested the existence of
numerous modifier genes (Kirpitchnikov 1999). Given that all
seven of these markers mapped into LG3, we inferred that a
gene cluster likely affected scale cover formation in common
carp. Six of the seven markers shared high homology (E-value
<e
5
) with zebrafish sequences, and five of them were in
syntenic regions in chromosome 8 of zebrafish (Table 2).
We identified six candidate genes for scale cover in the
syntenic regions (Table 3). Rohner et al. (2009) have reported
the requirement for fgfr1a in scale development. Fibroblast
growth factor (FGF) is the ligand for the fibroblast growth
factor receptor (FGFR). The atoh1a gene was reported to be
involved in the morphogenesis of the posterior lateral line
primordium in zebrafish and a Wnt-dependent FGF signaling
center was also found to participate in this process (Matsuda
and Chitnis 2010). The expression of atoh1a inhibits the
expression of fgfr1 (Matsuda and Chitnis 2010), which has
been demonstrated to be relevant to scale formation. The
ptch1 gene is a member of the Hedgehog signaling family,
which is required for perichondral osteoblast differentiation in
zebrafish (Felber et al. 2011). The bmp1a gene is important for
bone formation and stability (Asharani et al. 2012). It has been
often reported that fish scale exhibits many structural and
physiological characteristics that are similar to mammalian
bone (De Vrieze et al. 2010; Yoshikubo et al. 2005). The
wnt5a gene induces the emerging of limb buds by helping to
establish the cell polarity that may underlie the oriented cell
behaviors (Wyngaarden et al. 2010). These six genes were
identified based on the location of the five markers, FGFR1,
FGFR7, HLJ2509, HLJ3675, and HLJ3766, that were signif-
icantly correlated with scale cover.
Application in marker-assisted selection
Generally speaking, two years or more are necessary for
sexual maturity in most fish (Keenlyne and Jenkins 1993;
Morita and Fukuwaka 2007). Thus, conventional breed-
ing is a time-consuming task. Scale is a traditional phe-
notype that has been used in breeding programs and it
could serve as a selection target during domestication.
For the mirror scale recessive character, only the homo-
zygotes were selected, while for the scale dominant char-
acter, heterozygotes were selected, which results in more
generations for fixing the trait (Kirpitchnikov 1999). For
the application of MAS and MAI in breeding programs,
a large number of loci that influence targeted traits in
domesticated animals (e.g., pig and cattle) and food
crops (e.g., wheat and rice) have been identified
(Andersson et al. 1994; Georges et al. 1995; Elouafi
et al. 2001; Kwon et al. 2001).
In this study, seven SSRs that showed significant correla-
tion with scale cover pattern were identified. The verification
results confirmed that the seven SSRs were also significantly
correlated with scale cover pattern in the two validation
groups (P<0.01), except for FGFR1 and HLJ3227 in popula-
tion 3. We suggest that the different behaviors of these
markers in population 3 may be because of differences in the
family background or the smaller size of that population. We
found that 90 % of the P-values showed that the correlations
were significant and five of the markers showed significant
correlations in all three populations. This high accuracy will
strengthen the validity of their application in MAS and MAI.
In summary, the molecular mechanism of scale cover is
complex. Our results may contribute to understanding the
scale cover mechanism. In addition, the seven markers found
to be associated with scale cover pattern could be used for
breeding new varieties of common carp using MAS and MAI.
Acknowledgments This study was supported by grants from the Na-
tional High Technology Research and Development Program of China
(no. 2011AA100402-5), the China Ministry of Agriculture 948 Pro-
gram (no. 2011-G12), and the Special Scientific Research Funds for
Central Non-profit Institutes, Chinese Academy of Fishery Sciences
(no. 2014A05CG01).
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