Scientia Agricultura Sinica ›› 2018, Vol. 51 ›› Issue (22): 4373-4386.doi: 10.3864/j.issn.0578-1752.2018.22.015

• ANIMAL SCIENCE·VETERINARY SCIENCE·RESOURCE INSECT • Previous Articles     Next Articles

RNA-seq Analysis on Development Arrest of Duck Pectoralis Muscle During Semi-Late Embryonic Period

LIU HongXiang(),XU WenJuan(),ZHU ChunHong,TAO ZhiYun,SONG WeiTao,ZHANG ShuangJie,LI HuiFang()   

  1. Jiangsu Institute of Poultry Sciences, Yangzhou 225125, Jiangsu
  • Received:2017-08-03 Accepted:2018-09-12 Online:2018-11-16 Published:2018-11-16

Abstract:

【Objective】 In order to find the molecular varying mechanism involving the development arrest of pectoralis, Chinese native breeds, including Gaoyou Duck (GYD) and Jinding Duck (JDD), were selected for RNA-seq study using the pectoralis samples during the semi-late embryonic period.【Method】3 ducks of GYD and JDD , respectively, in the 21th embryonic day (ed21) and ed27 were selected to collect pectoralis major muscle and to extract total RNA to build cDNA library for RNA-seq with HiseqTM2000 of Illumina. At last, bioinformatics methods were used to extract differentially expressed genes (DEGs) between different breeds and time points, and to analyze the gene function annotation for studying molecular mechanism of pectoralis development retardation during ed21 and ed27. 【Result】 The results showed that the base ratios with quality value higher than 20 in reads (Q20) were more than 94%, and the base ratios of Q30 were more than 89%, which indicated a reliable sequencing result for the following analysis. The RNA level correlation inspection and mRNA expression level cluster graph both manifest that the correlation of mRNA expression patterns of GYD and JDD at ed21 or ed27 were higher than that of GYD (JDD) during ed21 and ed27. The numbers of DEGs between ed21 and ed27 (6128 DEGs for GYD and 6452 DEGs for JDD) were both apparently more than the numbers of DEGs between GYD and JDD in ed21 (522 DEGs) and ed27 (299 DEGs). qRT-PCR results of selected genes showed a strong correlation with RNA-seq results. GO and KEGG enrichment analysis showed the results that the genes involved in energy metabolism (mainly was coenzyme Q related genes, ATP enzymic synthesis related genes, and cytochrome C related genes) up regulated and DNA replication and cell cycle related-genes (mainly was minichromosome maintenance complex related genes and replication factor C related genes) down regulated significantly. This varies of related genes expression might relate to the slow myoblast proliferation and gradually exit the cell cycle to prepare for the next stage of fusing to multi-nuclei myotube and form myofiber. In the key genes involving in muscle growth and development, IGF1 (a gene promoting muscle growth) and MyoG (inducing terminal differentiation of myoblast) both down regulated dramatically. However, MUSTN1 gene, accelerating muscle fibre into differentiation and fusing stage, and MyoD gene, promoting muscle progenitor cell differentiated to myoblast, were expressed in a higher level in ed27 than in ed21. 【Conclusion】 A lot of genes differentially expressed between ed21 and ed27 in pectoralis muscle of duck, among of which the up-regulation of energy metabolism related genes, the down-regulation of DNA replicate and cell cycle related genes, and up-regulated MUSTN1, down-regulated IGF1 and MyoG, might closed relate to arrest phenomenon of pectoralis development during the semi-late stage of duck embryos.

Key words: duck, pectoralis muscle development, RNA-seq, differentially expressed genes

Table 1

Genes and primers designed for qRT-PCR validating"

基因
Gene
上游引物
Up-primer
下游引物
Lower-primer
产物长度
Product length (bp)
退火温度
Temperature (℃)
F16P1 CCCTAAAGGAAAGCTGAGAC CTCGGGCACTATATCCAGTA 115 60
COL1A1 GCCAACGAAATCGAGATCAG CGTCTTTGTCGTCTTGTACT 126 60
WIPI1 GAAATCCCAGATGTTTACATCG TCCGTCCCTTTCTTGAAGT 113 60
ARMC3 TTGGCATTGGCTGTAGTTTAG TACTCTTGAGGAGGAAGCAGAA 115 60
CEA20 TCTCCGAGCCAGAAATCC TCTTCCACCAGTACACGTC 105 60
GLIS3 ATGACGCAGAGACAAACT TTGTGTTGTACGTTCTTCTGAG 188 60
SRSF4 CTCTTACTCCAGAAGCCGA GATCTACTCTTGGAGCGAC 105 60
LAMC3 GAGGCCCAGAAGAAGATCA ACAACCTGTGCCCTCTTA 131 60
TNNI1 CTGCACGAGAAGGTTGAG GCAGGTCAAGCACTTTGAT 109 60
TNNT2 TCTCCAACATGCTGCATT CTGAGGTGGTCGATGTTC 130 60
TNNC1 ATGCTGCTTTAACTGGAATG CACCACAGGGTGGAAATC 179 60
MYOZ1 CAGAAGATTCAGTCTCACAAGT AGGTCTTTATCCAAGCCAC 103 60
MYBPH TCATGGGCAACACCTACTC GGATCTTCTCTGGCTGGTAA 129 60
COEA1 CTTCCTGCCAGCAATTAC AGCCAAACACTTCCATCATA 134 60
KCRS GACCAGTGCATCCAAACC TCTCAGCAAACACCTCGTAG 103 60
DEP1A ATCTGTTGTTTGTTGCTTCC TGTATCATCAAAGAGCGTGTG 134 60
ACTB* TGAGAGTAGCCCCTGAGGAGCAC TAACACCATCACCAGACTCCATCAC 198 60
GAPDH* CTTCGGAATAGGGAGGAGAC CGGAGATGATGACACGCTTA 131 60

Table 2

The statistical results of sequencing data"

品种 Breeds 样品 Sample 总碱基数(Gbp)Total nucleotides Q20(%) Q30(%) GC(%)
高邮鸭
GY
21胚龄 21 ed 5.45 94.42 89.55 51.47
27胚龄 27 ed 6.25 94.34 89.46 51.89
金定鸭
JD
21胚龄 21 ed 6.16 94.28 89.37 50.11
27胚龄 27 ed 5.79 94.33 89.37 51.42

Table 3

The results of transcriptome sequencing data"

项目
Statistical content
品种
Breeds
21胚龄 21 ed 27胚龄 27 ed
数量 Number 百分比 Percentage 数量 Number 百分比 Percentage
总读段数
Total reads
高邮鸭/GY 43570695 - 50059412 -
金定鸭/JD 49264929 - 46361619 -
总比对数
Total mapped
高邮鸭/GY 26927881 61.80 29480876 58.89
金定鸭/JD 31722102 64.39 27119296 58.50
多次比对数
Multiple mapped
高邮鸭/GY 560376 1.29 668497 1.33
金定鸭/JD 636927 1.29 603064 1.30
唯一比对数
Uniquely mapped
高邮鸭/GY 26367505 60.51 28812378 57.56
金定鸭/JD 31085175 63.10 26516232 57.19

Fig. 1

correlation check on RNA-seq level between samples"

Fig. 2

Cluster analysis of mRNA differentially expressed genes"

Table 4

RPKM values of PM tissue in different embryonic days"

品种
Breeds
RPKM值
RPKM value
0-1 1-3 3-15 15-60 > 60 总计
Total
高邮鸭
GY
21胚龄 21 ed 5197(27.22%) 2114(11.07%) 5245(27.47%) 4711(24.67%) 1828(9.57%) 19095
27胚龄 27 ed 5757(30.15%) 2186(11.45%) 5053(26.46%) 4310(22.57%) 1789(9.37%) 19095
金定鸭
JD
21胚龄 21 ed 5144(26.93%) 2152(11.27%) 5254(27.51%) 4744(24.84%) 1802(9.44%) 19095
27胚龄 27 ed 5884(30.81%) 2166(11.34%) 4894(25.63%) 4356(22.81%) 1796(9.40%) 19095

Fig. 3

Valcano chart of mRNA differentially expressed genes Numbers higher than 1.3 in Y-axis indicate padj<0.05"

Table 5

Correlations between RPKM ratios and ??Ct of genes expression profiles by qRT-PCR"

基因名
Gene symbol
相关系数
Correlation coefficient
描述
Description
F16P1 0.81 果糖-1,6-二磷酸酶1 Fructose-1,6-bisphosphatase 1
COL1A1 0.79 胶原蛋白α-1(I)链 Collagen alpha-1(I) chain
WIPI1 0.87 WD重复区域磷酸肌醇互作蛋白1 WD repeat domain phosphoinositide-interacting protein 1
ARMC3 0.88 Armadillo重复蛋白3 Armadillo repeat-containing protein 3
CEA20 0.89 癌胚抗原相关细胞粘附因子20 Carcinoembryonic antigen-related cell adhesion molecule 20
GLIS3 0.75 锌指蛋白GLIS3 Zinc finger protein GLIS3
SRSF4 0.79 富含丝氨酸/精氨酸剪切因子 Serine/arginine-rich splicing factor 4
LAMC3 0.82 层连蛋白亚基γ3 Laminin subunit gamma-3
TNNI1 0.96 慢肌中肌钙蛋白1 Troponin 1, slow skeletal muscle
TNNT2 0.81 心肌型肌钙蛋白2 Troponin T2, Cardiac Type
TNNC1 0.70 慢肌和心肌中肌钙蛋白C Troponin C, slow skeletal and cardiac muscles
MYOZ1 0.76 Myozenin蛋白1 Myozenin-1
MYBPH 0.72 Myosin结合蛋白H Myosin-binding protein H
COEA1 0.87 胶原蛋白α-1(XIV)链 Collagen alpha-1(XIV) chain
KCRS 0.82 线粒体中S型肌酸激酶 Creatine kinase S-type, mitochondrial
DEP1A 0.75 含DEP区域蛋白1A DEP domain-containing protein 1A

Table 6

The change of skeletal muscle related genes mRNA expression level"

基因登录号
GeneID
基因名
Gene symbol
比较对象
Objects compared
前一时间
Before
后一时间
After
log2(差异倍数)
log2(FoldChange)
校正p值
padj
原始p值
pval
上/下调
Up or down
ENSAPLG00000010676 IGF1 高邮鸭21、27胚龄
GY21v27
95.09 25.38 -1.91 1.41E-07 1.23E-08 下调Down
金定鸭21、27胚龄
JD21v27
95.24 25.00 -1.93 2.02E-07 1.91E-08 下调Down
ENSAPLG00000004095 MUSTN1 高邮鸭21、27胚龄
GY21v27
2652.05 19892.66 2.91 6.81E-11 3.73E-12 上调Up
金定鸭21、27胚龄
JD21v27
2066.24 11844.22 2.52 1.86E-33 1.78E-35 上调Up
ENSAPLG00000012230 MSTN 高邮鸭21、27胚龄
GY21v27
1281.81 825.70 -0.63 0.53 0.34 下调Down
金定鸭21、27胚龄
JD21v27
967.86 483.89 -1.00 0.08 0.03 下调Down
ENSAPLG00000005673 MyoD1 高邮鸭21、27胚龄
GY21v27
3800.16 6924.07 0.87 3.39E-04 5.70E-05 上调Up
金定鸭21、27胚龄
JD21v27
4074.60 6240.65 0.62 0.01 2.65E-03 上调Up
ENSAPLG00000001996 MyoG 高邮鸭21、27胚龄
GY21v27
870.47 23.75 -5.20 1.39E-100 9.27E-104 下调Down
金定鸭21、27胚龄
JD21v27
864.99 51.91 -4.06 2.58E-73 5.01E-76 下调Down

Fig. 4

GO function classification of mRNA differentially expressed genes of GY and JD between 21 ed and 27 ed"

Table 7

The same GO terms of GY and JD enriched significantly between DEGs between 21 ed and 27 ed"

GO类型
GO type
GO条目号
GO terms
GO描述
GO description
标记
Mark
共有基因数
Number of shared genes
上/下调
Up or down
生物过程
Biological process
GO:0007018 基于微管的运动 microtubule-based movement B3 24 下调Down
GO:0007049 细胞周期 cell cycle B4 86 下调Down
细胞组分
Cellular component
GO:0005739 线粒体 mitochondrion C1 53 上调Up
GO:0031012 细胞外基质 extracellular matrix C4 57 下调Down
GO:0043228 无膜细胞器 non-membrane-bounded organelle C6 161 下调Down
GO:0043232 细胞内无膜细胞器 intracellular non-membrane-bounded organelle C7 161 下调Down
分子功能
Molecular function
GO:0003774 马达运动 motor activity M2 48 下调Down
GO:0003777 微管马达运动 microtubule motor activity M3 24 下调Down
GO:0005198 结构分子活性 structural molecule activity M4 137 下调Down
GO:0008017 微管结合 microtubule binding M5 25 下调Down
GO:0008094 DNA依赖的ATP酶活性 DNA-dependent ATPase activity M7 17 下调Down
GO:0015631 微管蛋白结合 tubulin binding M8 26 下调Down
GO:0016817 作用于酸酐的水解酶活性hydrolase activity, acting on acid anhydrides M11 178 下调Down

Fig. 5

KEGG function classification of mRNA differentially expressed genes of GY and JD between 21 ed and 27 ed"

Table 8

The same KEGG pathways of GY and JD enriched significantly between DEGs between 21 ed and 27 ed"

KEGG通路
KEGG pathway
KEGG描述
KEGG description
标记
Mark
共有基因数
Number of shared genes
上/下调
Up or down
apla00020 三羧酸循环(TCA循环) Citrate cycle (TCA cycle) Term2 17 上调Up
apla00190 氧化磷酸化 Oxidative phosphorylation Term6 64 上调Up
apla01200 碳的代谢 Carbon metabolism Term9 34 上调Up
apla03030 DNA复制 DNA replication Term12 16 下调Down
apla04110 细胞周期 Cell cycle Term15 36 下调Down

Table 9

The shared genes by results of GO and KEGG analysis"

基因名
Gene name
基因描述
Gene description
Ensembl No. 上/下调
Up or down
基因名
Gene name
基因描述
Gene description
Ensembl No. 上/下调
Up or down
ATP5F1 ATP合成酶:H+转运线粒体Fo复合物亚基5F1
ATP synthase, H+ transporting, mitochondrial Fo complex subunit 5F1
ENSAPLG00000013428 上调
Up
ANAPC2 (细胞分裂)后期启动复合物亚基2
Anaphase promoting complex subunit 2
ENSAPLG00000001836 下调Down
ATP5H ATP合成酶:H+转运线粒体Fo复合物亚基5H
ATP synthase, H+ transporting, mitochondrial Fo complex subunit 5H
ENSAPLG00000006404 上调
Up
DNA2 DNA复制解螺旋/核酸酶2
DNA replication helicase/nuclease 2
ENSAPLG00000015576 下调Down
ATP5J ATP合成酶:H+转运线粒体Fo复合物亚基5J
ATP synthase, H+ transporting, mitochondrial Fo complex subunit 5J
ENSAPLG00000009600 上调
Up
FEN1 Flap结构特异性核酸内切酶1
Flap structure-specific endonuclease 1
ENSAPLG00000001725 下调Down
COX5A 细胞色素c氧化酶亚基5A
Cytochrome c oxidase subunit 5A
ENSAPLG00000014886 上调
Up
MAD1L1 MAD1有丝分裂阻滞缺陷类似物1
MAD1 mitotic arrest deficient like 1
ENSAPLG00000015788 下调Down
COX7A2L 细胞色素c氧化酶亚基类7A2
Cytochrome c oxidase subunit 7A2 like
ENSAPLG00000012898 上调
Up
MCM2 微型染色体维持复合物组分2
Minichromosome maintenance complex component 2
ENSAPLG00000004520 下调Down
LOC101800937 线粒体中细胞色素c氧化酶亚基7B
Cytochrome c oxidase subunit 7B, mitochondrial
ENSAPLG00000007286 上调
Up
MCM3 微型染色体维持复合物组分3
Minichromosome maintenance complex component 3
ENSAPLG00000013058 下调Down
NDUFA5 NADH:泛醌氧化还原酶亚基A5
NADH: Ubiquinone oxidoreductase subunit A5
ENSAPLG00000014770 上调
Up
MCM4 微型染色体维持复合物组分4
Minichromosome maintenance complex component 4
ENSAPLG00000003491 下调
Down
NDUFA7 NADH:泛醌氧化还原酶亚基A7
NADH: Ubiquinone oxidoreductase subunit A7
ENSAPLG00000011378 上调
Up
MCM5 微型染色体维持复合物组分5
Minichromosome maintenance complex component 5
ENSAPLG00000007931 下调
Down
NDUFB1 NADH:泛醌氧化还原酶亚基B1
NADH: Ubiquinone oxidoreductase subunit B1
ENSAPLG00000006000 上调
Up
ORC5 起点识别复合物亚基5
Origin recognition complex subunit 5
ENSAPLG00000002905 下调
Down
NDUFB3 NADH:泛醌氧化还原酶亚基B3
NADH: Ubiquinone oxidoreductase subunit B3
ENSAPLG00000015508 上调
Up
POLE DNA聚合酶ε催化亚基
DNA polymerase epsilon, catalytic subunit
ENSAPLG00000009950 下调
Down
NDUFB4 NADH:泛醌氧化还原酶亚基B4
NADH: Ubiquinone oxidoreductase subunit B4
ENSAPLG00000007537 上调
Up
RB1 RB转录共阻遏因子1
RB transcriptional corepressor 1
ENSAPLG00000007734 下调
Down
NDUFB8 NADH:泛醌氧化还原酶亚基B8
NADH: Ubiquinone oxidoreductase subunit B8
ENSAPLG00000015152 上调
Up
RFC1 复制因子C亚基1
Replication factor C subunit 1
ENSAPLG00000010594 下调
Down
NDUFC2 NADH:泛醌氧化还原酶亚基C2
NADH: Ubiquinone oxidoreductase subunit C2
ENSAPLG00000006009 上调
Up
RFC2 复制因子C亚基2
Replication factor C subunit 2
ENSAPLG00000009389 下调
Down
NDUFS6 NADH:泛醌氧化还原酶亚基S6
NADH: Ubiquinone oxidoreductase subunit S6
ENSAPLG00000014333 上调
Up
TFDP1 转录因子Dp-1
Transcription factor Dp-1
ENSAPLG00000014438 下调
Down
SDHD 琥珀酸盐脱氢酶复合物亚基D
Succinate dehydrogenase complex subunit D
ENSAPLG00000005936 上调
Up
YWHAZ 酪氨酸3-单氧酶/色氨酸5-单氧酶活化蛋白ζ
Tyrosine 3-monooxygenase/tryptophan 5-monooxygenase activation protein zeta
ENSAPLG00000002635 下调
Down
UQCRB 泛醌-细胞色素c还原酶结合蛋白
Ubiquinol-cytochrome c reductase binding protein
ENSAPLG00000012746 上调
Up
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