Download Polymorphism of FecB Gene in Nine Sheep Breeds or Strains and

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ISSN 0379-4172
Acta Genetica Sinica, February 2006, 33 (2)：117–124
Polymorphism of FecB Gene in Nine Sheep Breeds or Strains
and Its Effects on Litter Size, Lamb Growth and Development
GUAN Feng1,4, LIU Shou-Ren2, SHI Guo-Qing1, 2, AI Jun-Tao1, MAO Da-Gan1,
YANG Li-Guo1,3,①
1. Research Institute of Animal Breeding & Reproduction, Nanjing Agricultural University, Nanjing 210095, China;
2. Institute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural Reclamation, Shihezi 832000, China;
3. College of Animal Science, Huazhong Agricultural University, Wuhan 430070, China
4. College of Life Sciences, China Jiliang University, Hangzhou 310018, China
Abstract: Nine sheep breeds or strains, including 615 individuals were screened with forced PCR RFLP method for the FecB gene
to study the polymorphism and its effects on litter size, body weight and body size. Results showed that the polymorphism frequencies of FecB gene were significantly imbalanced in these breeds or strains. The Hu sheep were all homozygous carriers of FecB
gene(BB). In the Chinese Merino prolific meat strain, the genotype frequencies of BB, B+ and ++ were 51%, 30% and 19%, respectively, whereas all the other flocks had only the wild-type (++) genotype. Results within the Chinese Merino prolific meat strain
showed that the mean litter size of ewes with genotype BB and B+ were 2.8 (±0.74) and 2.3 (±0.63) (P<0.05), whereas ++ genotype
ewes had a litter size of only 1.2 (±0.68) (P<0.01). At day 90 after birth, the body weights of BB/B+ genotype lambs were higher
than that of ++ genotype lambs (18.6±3.70 kg, 18.0±3.71 kg vs 15.6±2.22 kg, P<0.05). In addition, the heart girth and chest width
of BB/B+ genotype lambs were significantly longer than those of the ++ lambs (P<0.05). No significant differences were observed
in either body weight or body size at day 120. Litter size at first lambing from Hu at Natural Source Conservative Region was
found to be significantly higher than that from the other two regions sampled (P<0.05). In addition to the additive effect on litter
size, these findings showed for the first time that the FecB gene had a positive effect on early postnatal body growth.
Key words: sheep; FecB gene; litter size; body weight; body size
Litter size and lamb growth are important economic traits in sheep breeding and reproduction. Recently, it has been reported that bone morphogenetic
protein receptor IB (BMPR-IB) gene mutation was
responsible for the high prolificacy associated with
the FecB gene in Booroola Merino sheep [1-3]. This
mutation is located in the highly conserved kinase
domain of BMPR-IB, and mutant sheep are characterized by ‘precocious’ differentiation of ovarian follicles, leading to the production of large numbers of
ovulatory follicles that are smaller in diameter than
wild-type follicles [4]. This mutation can be detected
directly by a forced PCR restriction fragment length
polymorphism (RFLP) approach based on the reports
described by Souza et al. [2] and Davis et al [5].
In recent years, many aspects of the FecB gene,
including reproductive endocrinology
[6]
, ovarian de-
[7]
velopment , litter size, organ development and body
mass
[8]
have been studied. This gene has additive
effect on litter size and ovulation rate, but has negative effect on fetal growth and development and body
mass during gestation. For example, body weights
Received: 2004-11-30; Accepted: 2005-04-03
This work was supported by the Natural Science Foundation of Zhejiang Province of China (No.Y 305107) and Shanghai Key Project of Science and Technology Service for Agriculture(No.2002, 1-3-6).
①
Corresponding author.Tel: +86-27-8728 1813; E-mail: [email protected]
118
Acta Genetica Sinica
遗传学报
were lighter (P<0.05) at most gestational ages in
BB/B+ than in ++ fetuses
[6]
ral Resource Conservative Region in 1982 and after
[9]
several generations of strict selection, its litter size
.
It was reported that FecB gene had been detected
in Hu
Since the establishment of Dongshan Hu-sheep Natu-
, and crown-rump length
was shorter in BB/B+ than in ++ fetuses
[10]
Vol.33 No.2 2006
and small tailed Han
[11]
in China, and that it
could be a major gene affecting the litter size of small
tailed Han sheep.
Both Hu and Small Tailed Han are Chinese breeds
that are among the most prolific sheep breeds in the
world [12]. Several sheep breeds have been introduced
into China in recent years and crossed with local
sheep. The distribution of the FecB mutation of the
BMPR-IB gene and its effects on body weight and
body sizes in these sheep flocks are unknown. The
objective of this paper is to study the frequency distributions of FecB in different breeds or strains in
China, and evaluate the effects of the FecB gene on
(2.256 vs 2.567) and body weight have improved significantly (P<0.05)[15].
Chinese Merino prolific meat strain has been
bred by Xinjiang Academy of Agricultural Reclamation since 1981, via reciprocal crossing of Hu with
Chinese Merino fine wool prolific flocks on the basis
of phenotype selection. After several generations of
selection, the strain has stabilized to being 1/4 Hu and
3/4 Chinese Merino.
1. 2
Primer synthesis and PCR-RFLP reactions
Primers were synthesized by Shanghai Sangon
Biotech Co. Ltd based on the sequences described by
Wilson et al
[3]
. DNA tests were carried out using
litter size, and body weights and body sizes after birth.
forced PCR RFLP based on the method described by
1
Forward primer: 5′-CCAGAGGACAATAGCAAAG-
Davis et al [5]. The primers were designed as follows:
Materials and Methods
1. 1
CAAA-3′; Reverse primer: 5′-CAAGATGTTTTCAT-
Experimental sheep flocks and sampling
GCCTCATCAACAGGTC-3′.
A total of 615 sheep individuals were examined
The reverse primer deliberately introduced by a
in this study from nine breeds or strains, including Hu,
point mutation which would create an AvaⅡ restric-
Suffolk, Dorset, Charolais, Chinese Merino prolific
tion site (G|GACC) in PCR products from FecB car-
meat strain, Romney Hills, Merino, and crossbreed of
rier sheep, whereas PCR products from the noncarri-
Suffolk × Chinese Merino as well as Dorset × Chi-
ers lacked this site.
nese Merino. Hu-sheep samples were collected from
Genomic DNA (50-100 ng) was used in a 20 μL
farms in central production areas including farms in
of reaction volume. The amplification was carried out
Shanghai, Suzhou and Dongshan Hu-sheep Natural
by 30 cycles at 94℃ for 30 s, 60℃ for 30 s, and 72℃
Resource Conservative Region in Jiangsu province.
for 30 s followed by 72℃ for 5 min. The PCR prod-
The other breeds were sampled from Xinjiang Agri-
ucts were digested with AvaⅡ (Dalian TaKaRa Bio-
culture No.6 Sheep Farm.
After sterilization with 70% ethanol about 5 g of
skin tissue was cut from the ovine ear with a clamp.
All samples were taken back to the laboratory under
low temperature. The genomic DNA was extracted
according to methods described by Molecular Cloning
[13]
, and stored at -20℃ before use.
tech Co.,Ltd, China) overnight at 37℃, and the resulting products were separated by 12% PAGE gel
and visualized with silver staining.
1. 3
Genotype analysis
The forced PCR of the FecB gene produced a
190 base pair (bp) band. The FecB gene homozygous
The Hu is the predominant breed in Suzhou,
carriers could be identified as having a 160 bp band
Shanghai and Dongshan where they are well adapted
(BB), the noncarriers as having a 190 bp band (++),
to the hot and humid environment. Dongshan, near the
whereas and the heterozygotes as having both the 160
Tai lake, is one of the original sources of Hu-sheep
[14]
.
and 190 bp bands (B+).
GUAN Feng et al.: Polymorphism of FecB Gene in Nine Sheep Breeds or Strains and Its Effects on Litter Size,……
1. 4
Statistical analysis
All the records of body sizes and weights were
measured according to methods described by LIU
Zhen-Yi [16]. All data including mean litter size were
presented as x ±SD. The non-informative individuals were excluded. Body weight and body size data
were analyzed by one-way ANOVA.
119
Table 1 Frequency distributions of FecB gene in nine
sheep breeds or strains
No. of
samples
Breed or strain
Genotype frequency
BB
B+
++
Hu sheep
305
1
0
0
Chinese Merino prolific
Meat strain
53
0.51
0.30
0.19
Suffolk sheep
22
0
0
1
Dorset sheep
56
0
0
1
Charolais sheep
21
0
0
1
Suffolk×China Merino
36
0
0
1
Dorset×China Merino
49
0
0
1
Results of FecB gene PCR products after AvaⅡ
China Merino
24
0
0
1
digestion can be seen in Fig.1. Thus this PCR-RFLP
technique can be used to detect and genotype FecB
gene clearly.
Romney Hills
49
0
0
1
2
Results
2. 1
Results of PCR-RFLP electrophoresis
2. 3
Comparison of litter size
To eliminate error from different breeds and
strains and other effects, comparison of litter size,
body weight and body size was confined to the Chinese Merino prolific meat strain. Within this strain,
the litter size of ewes with the BB genotype averaged
2.84±0.74, which was significantly greater than that
Fig. 1
PCR-RFLP genotyping of FecB gene in sheep
Lanes 1-3 and 5-9 are AvaⅡ-digested PCR products of either
190 bp (representing genotype ++) or 160 bp (genotype BB);
Lane 4 is the pBR322/MspⅠ DNA Marker (labeled as M).
2. 2
Frequency distributions of FecB gene in different breeds or strains
A total of 615 individuals from nine different breeds
or strains were screened by the forced PCR-RFLP approach. Results (Table 1) showed that the frequency
of polymorphism distributions of FecB gene was
most imbalanced in these breeds or strains. Chinese
Merino prolific meat strain had three different
Booroola genotypes (BB, B+ and ++), and their frequencies were 51%, 30% and 19%, respectively. In
contrast, Hu were all homozygous for FecB (BB)
whereas the other breeds all had the wildtype allele
(++). In addition, we found that Hu-sheep crossbred
progenies had a B+ genotype, which exhibited a simple Mendelian pattern of segregation when they were
backcrossed.
of ewes with the ++ genotype (1.23±0.68, P<0.01,
Table 2). The ewes with the BB genotype also produced 0.5 lambs more than ewes with the B+ genotype, although the difference was not statistically significant.
Table 2 Comparison of litter size among three genotypes
of Chinese Merino meat-prolific strain ewes at parity
Genotype
BB
B+
++
No. of sample
27
16
10
Mean litter size
2.84±0.74A
2.34±0.63A
1.23±0.68B
Note: In this table and throughout, values (mean ± SD)
in the same line with different superscripts are statistically
different from each other, with small letters indicating
P<0.05 and with capital letter indicating P<0.01.
2. 4
Body weight and body size in flocks with
different genotypes
Body weight and body size are important indices of body growth and breeding traits. In this study,
the results showed that the mean body weight of BB
120
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2. 5
Table 3 Comparison of body weight of ewes at ages 90
and 120 days among three genotypes
BB
B+
++
27
16
10
Birth weight(kg)
3.4±0.47
3.4±0.87
3.3±0.78
Body weight(kg)
at 90 days
18.6±3.70a
18.0±3.31a
15.6±2.22b
Body weight(kg)
at 120 days
23.5±4.95
23.0±5.00
22.6±3.68
No. of samples
3
Discussion
RFLP is a rapid, simple and exact technique
Comparison of body size at ages 90 and 120 days
Genotype
No. of sample
Age
Litter size among Hu-sheep from different
sources in China
The results of genotyping in this study are fully
consistent with previous studies in our laboratory [10].
There was no difference in total mean litter size among
the different flocks in the three sample sources (Table
5). And no difference was detected between the second
and the third lambing, but in Dongshan Hu sheep
Natural Resource Conservative Region, the mean litter
size at first lambing was significantly higher than that
of sheep from the other two regions (P<0.05).
The differences in heart girth and chest width
were only significant between the flocks with carrier (BB/ B+) and noncarrier (++) genotypes at 90
Table 4
Vol.33 No.2 2006
days of age (P<0.05, Table 4). There were no significant differences among different genotypes in
other body size measures at 90 days or in any parameters at 120 days.
and B+ lambs were significantly higher (P<0.05) than
that of ++ lambs at 90 days of age (Table 3). No
significant differences were found between either BB
and B+ or B+ and ++ flocks by day 120.
Genotype
Acta Genetica Sinica
B+
++
27
16
10
90
120
90
120
90
120
Body length (cm)
53.6±3.82
55.6±3.90
54.0±4.88
55.6±4.08
50.4±2.94
55.6±3.91
Body height (cm)
53.6±3.43
55.8±4.24
52.5±4.20
55.7±3.77
50.6±2.88
55.6±3.67
Heart girth (cm)
63.8±4.62a
69.1±6.29
61.2±4.42a
69.3±6.34
58.6±3.21b
68.4±6.16
Chest depth (cm)
23.1±2.08
26.0±2.00
22.1±1.75
25.8±1.90
21.1±1.78
25.8±1.87
Chest width (cm)
16.0±1.33
a
17.6±1.71
16.0±1.10
a
17.5±1.69
14.6±1.31
b
17.4±1.63
Cannon girth (cm)
6.9±0.44
7.2±0.53
6.9±0.65
7.1±0.39
6.6±0.48
Table 5
(days)
BB
7.1±0.41
Comparison of litter size in different sources of samples
Source of samples
No. of sample
Litter size at 1-3 lambing
Suzhou
Shanghai
Dongshan
Total
91
67
87
245
2.21±1.00
2.10±0.74
2.37±0.74
2.24±0.87
Mean litter size at 1st lambing
1.90±0.90
a
1.78±0.64
a
2.12±0.67
b
1.92±0.73a
Mean litter size at 2nd lambing
2.43±0.95
2.23±0.75
2.56±0.62
2.45±0.87
Mean litter size at 3rd lambing
2.54±1.11
2.36±0.50
2.80±1.01
2.56±1.00
GUAN Feng et al.: Polymorphism of FecB Gene in Nine Sheep Breeds or Strains and Its Effects on Litter Size,……
121
for single nucleotide polymorphism (SNP) genotyping.
After a forced restriction site was introduced into one
of the primers, the PCR product contained a certain
restriction enzyme site. This forced PCR-RFLP approach has been used previously to genotype prolific
sheep [2,5] and swine [17] to decide whether they had the
same mutation as FecB in Booroola Merino sheep.
In our experiments, we used such an approach
FecB mutation (Q249R) in BMPR-IB gene was
found, the ewes were classified as homozygous,
heterozygous and noncarriers and could be segregated on the basis of ovulation rate records of five or
more, three or four, and one or two, respectively [19].
But in our experiment, a forced PCR-RFLP method
was applied for genotyping.
It was reported that the FecB gene has negative
and PAGE to detect the genotypes based on the
effects on fetal body weight, body size and develop-
[5]
.
ment during pregnancy [6]. Body weights were lighter
Results in Fig. 1 show that this method could be used
at most gestational ages in BB/B+ than in ++ fetuses,
to accurately genotype the FecB gene. Illegible or
and the BB/B+ grew slowly and body lengths were
inconclusive results were repeated until the genotyp-
shorter than ++ fetuses. In contrast, when measuring
ing was clear, or they were excluded from the data
postnatal growth and development our results showed
analysis.
that by day 90 after birth, body weight, heart girth,
method described by Souza et al.
[2]
and Davis et al
It has been well known that Hu and Chinese
and body height were significantly increased in
Merino prolific meat sheep are highly prolific, and
BB/B+ compared with ++ lambs. The BB and B+
Chinese Merino and Romney Hills are more prolific
lambs of similar birth weight grew more in the first
in comparison with many other breeds. Findings
90 days after birth. The differences probably resulted
concerning Hu sheep that has only a single BB geno-
from the effects of different breeds and different
type are not in agreement with other reports about
phases of development, environmental conditions,
Booroola sheep, in which three genotypes have been
different lambing and nutrition, or other factors alto-
observed. The phenomenon probably resulted from
the whole process of Hu sheep establishment, result-
gether. The mechanism requires further research.
To date, in addition to BMPR-IB (FecB) and
ing in the gene being fixed in the Hu population, just
BMP15 gene mutations
as it has also been observed in some Garole sheep
of Booroola sheep and Inverdale or Hanna sheep,
populations in India [5].
there is evidence that other major genes or QTLs may
It was reported that the effect of FecB gene is
additive for litter size and ovulation rate, increasing
ovulation by about 1.65 per copy and litter size by 0.9
for one copy and a further 0.4 for two copies [18]. Our
results showed that based on litter size, the effect of
the FecB gene in Hu sheep and its crossbreds is similar to that reported in Booroola sheep. Although ovulation rates have not been measured in the Hu sheep,
the litter size effects are consistent with other studies
of the Booroola gene (FecB), which have shown that
it has a large effect on ovulation rate. The mean litter size previously reported in Booroola sheep is
higher than that of Chinese Merino prolific meat
strain and Hu sheep, which probably resulted from
different breeds, environments, maternal nutrition,
seasons and method for genotyping. Before the
be segregated from Icelandic sheep, Javanese sheep,
[20]
influencing ovulation rate
Olkuska, Cambridge, Lacaune, Belclare and Woodlands sheep breeds [21]. But BMP15 mutation has not
been found in most individuals in our study based on
the method described by Galloway et al
[20]
. The
Thoka gene has been found to be a major gene in
Iceland sheep, and has the similar mechanism with
FecB gene but not FecB or BMP15 genes
[5]
. The
Thoka gene has additive effect on ovulation, increasing ovulation rate by about 1.21 or more and
litter size by 0.6
[22]
. The FecJ gene was a major
gene segregating in Javanese thin tailed sheep and
has a smaller additive effect on litter size and ovulation rate than that of the FecB gene [23]. Davis et al. [5]
subsequently found that the FecJ gene was the same
mutation as FecB. The effect of a major gene on
122
mean litter size is likely to be influenced by breed,
environmental conditions, maternal nutrition and
other factors.
Muslant et al. [1] and Wilson et al. [3] reported that
FecB is a major gene inherited as a single autosomal
locus, which regulates ovulation rate of Booroola
sheep. Using DNA testing we also found that the FecB
gene followed Mendelian segregation patterns in Hu
sheep and crossbreds. Davis et al.[5] proposed the
Garole sheep of India as the ancestor of Australian
Booroola Merinos based on historical records and
evidence that they had the same BMPR-IB gene mutation. The Hu and its crosses were the only breeds in
our study that carried the FecB mutation. Research
has shown that the Hu and Han are closely related
and both descend from ancient Mongol Sheep [24].
We found that Hu-sheep have a higher litter size
at first lambing in Nature Source Conservative Region than those from the other two regions, which
probably resulted from the method of breeding. Traditionally, sheep were maintained in family flocks of
about three or four ewes, many families relying on
neighbors for a ram in a village. The aim of breeding
was high prolificacy and high quality of lambskins.
Ewes and rams were selected on the basis of these
traits because this region was famous for Hu-sheep
lambskins. Traditionally, the farmer sold excellent
individuals and retained lower quality individuals.
Later when exportation of lambskins was resisted in
1980s, the excellent individuals were retained, which
is the major reason for high prolificacy and fast
growth in this breed.
Hu have a single BB genotype, but the litter size
of the first lambing is significantly different between
Hu sheep from different flocks. Whether other gene(s)
or quantitative trait loci (QTL) regulating ovulation
are also present requires further research. We propose
that this difference probably is the consequence of
different environmental conditions, nutrition, selection, and possibly even QTL or gene(s) regulating
sexual maturity and ovulation rate.
Acknowledgement: We thank the farmers for collection of samples in Xinjiang Agriculture No.6 farm
遗传学报
Acta Genetica Sinica
Vol.33 No.2 2006
and Xinjiang Academy of Agricultural Reclamation
for providing the laboratory. We thank Mr. Davis GH
in NewZealand for advice and amending this paper.
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遗传学报
Acta Genetica Sinica
Vol.33 No.2 2006
FecB 基因在 9 个绵羊品种中的多态性及其与产羔数和羔羊生
长发育的相关性
管 峰 1,4，刘守仁 2，石国庆 1,2，艾君涛 1，茆达干 1，杨利国 1,3
1. 南京农业大学动物繁育研究所，南京 210095；
2. 新疆农垦科学院畜牧兽医研究所，石河子 832000；
3. 华中农业大学动物科技学院，武汉 430070;
4. 中国计量学院生命科学学院，杭州 310018
摘 要：以绵羊 BMPR-IB 基因为候选基因，应用 PCR-RFLP 方法通过分析湖羊、夏洛来、陶赛特、萨福克、罗米丽、中国
美利奴羊、中国美利奴肉用多胎品系以及陶赛特×中国美利奴羊和萨福克×中国美利奴羊杂交后代共 615 只个体的 FecB
基因多态性，以及 BMPR-IB 基因多态性对产羔数、体尺和体重的影响。结果表明，BMPR-IB 基因在不同品种（系）绵羊
中共有 3 种基因型（BB、B+和++），但基因型频率分布在各品种(系)间差异极显著(P<0.01)。在湖羊中仅有 BB 基因型；在
中国美利奴肉用多胎品系中 BB、B+和++基因型频率分别为 51%、30%和 19%；而其他品种（系）羊中则仅有++基因型。
对中国美利奴羊肉用多胎品系研究，发现 BB 和 B+基因型群体平均产羔数分别为 2.8 和 2.3，显著高于++基因型群体（1.2，
P<0.01）
。在 90 日龄时，BB 和 B+基因型群体的体重分别为 18.6±3.70 kg 和 18.0±3.31 kg，显著高于++基因型群体（15.6
±2.22 kg，P<0.05）；此外，90 日龄时，BB 和 B+基因型群体比++基因型群体胸围、胸宽较大（Ｐ<0.05）；但这些差异在
120 日龄时消失。另外，我们还发现不同地区群体的第一胎产羔数存在明显差别。这些结果表明，BMPR-IB 基因为影响绵
羊产羔数的主效基因，并首次证明该基因对后代羔羊出生后生长发育具有加性效应。
关键词：绵羊；BMPR-IB 基因；产羔数；体重；体尺
作者简介：管 峰（1977-），男，博士，研究方向：动物分子标记育种。现工作单位：中国计量学院生命科学学院