莱芜猪和大白猪背最长肌miRNA与mRNA转录组测序及特征分析
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摘要
猪不但可以作为重要的农业经济动物为人类提供大量的肉类产品，而且还可以作为模式生物用于医学研究。由于遗传背景及人工选育方式的不同，造成了中外猪种在生产性状方面存在很大的差异。比如，莱芜猪作为我国特有的猪种资源，具有肉质优良的种质特性；而西方猪种虽然在生长速度方面具有优势，但是其较差的肉品质已不满足于消费者的需求。大量研究证实中外猪种间种质差异的形成与基因的差异表达有关，因此，从转录组水平探索中外猪种骨骼肌差异表达基因，对于解析品种间的差异及揭示形成该差异的分子机理具有重要作用。
本研究选用生长速度慢但肉质优良的莱芜猪（Laiwu pig, LW）和生长速度快但肉质较差的大白猪（Yorkshire, YS）作为试验动物，利用高通量测序技术分析了莱芜猪与大白猪骨骼肌中的差异表达miRNA与差异表达基因，并对差异表达miRNA与基因进行筛选及信号通路富集，分析差异miRNA与差异基因在中外猪种中的功能。对于差异表达miRNA，采用生物信息学软件预测了这些miRNA可能的靶基因，构建了差异表达miRNA的调控网络图。为了验证高通量测序结果的正确性，我们采用qRT-PCR方法对差异表达miRNA与差异基因进行了定量验证，结果表明，高通量测序结果比较可靠。本研究的主要结果如下：
（1）莱芜猪与大白猪骨骼肌小RNA测序分析
分别构建了3个莱芜猪与3个大白猪的背最长肌小RNA文库，并利用RNA-seq技术对6个小RNA文库进行了测序，分析miRNA在莱芜猪与大白猪中的表达模式。结果表明，平均在每个莱芜猪的小RNA文库中获得了13,493,607的纯净测序reads，大白猪约为12,938,257。总共筛选出265个已知miRNA，其中有229个在6个文库中都表达；另外，还预测到94个新miRNA。对筛选出的359个miRNA进行表达分析，结果发现ssc-miR-1在两个品种猪中都是表达量最高的，而ssc-miR-194b-5p在两个品种猪中的差异倍数最大（6.35倍）；此外，还发现有25个miRNA在莱芜猪与大白猪骨骼肌中是显著差异表达（q <0.05）。在25个差异显著的miRNA中，有10个miRNA在莱芜猪中上调表达，15个下调表达。为了验证测序结果的准确性，随机选取了16个miRNA进行qRT-PCR验证，qRT-PCR结果与测序结果基本一致。对差异表达miRNA的靶基因进行预测，结果获得了10,806个靶基因，而这些靶基因主要被富集到代谢过程等信号通路中。
（2）莱芜猪与大白猪骨骼肌mRNA转录组测序分析
为了研究莱芜猪与大白猪骨骼肌全基因组的转录谱，利用RNA-seq技术对构建的两个品种猪骨骼肌文库进行测序，测序结果显示在莱芜猪的文库中获得了40,498,476的测序reads，大白猪为59,072,892；其中，80%以上的测序reads可以比对到猪的基因组中。在两个文库中共检测到12种选择性剪切类型分析，其中以TSS（转录起始位点）与TTS（转录终止位点）两种剪切类型所占的比例最大，分别占到43%和40%以上。通过对测序reads进行比对分析，结果显示在莱芜猪与大白猪骨骼肌中有10,482个共表达基因，另有739个基因只在莱芜猪中表达，712个基因只在大白猪中表达。在两个品种猪中总共预测得到1,678个新基因，其中对应2,229个新转录本。为了更进一步研究这些差异基因的功能，对这些差异基因进行检验分析，结果表明在莱芜猪与大白猪骨骼肌中有178个显著差异表达的基因（q <0.05），其中，相对于大白猪，在莱芜猪中有98个差异基因为上调表达，80个下调表达。为了验证这些差异基因的正确性，随机选取了12个差异表达基因进行qRT-PCR验证，测序结果与qRT-PCR结果基本一致，两者具有很强的相关性（R2=0.93）。对差异表达基因进行功能注释，发现差异表达基因主要被富集到代谢通路，尤其是与脂肪代谢相关的信号通路，比如脂肪酸合成代谢通路等。
（3）骨骼肌差异miRNA与差异基因关联分析
为了从整个转录水平了解两个品种猪差异表达miRNA及差异基因的功能，对178个差异表达基因与25个差异表达miRNA进行关联分析，结果表明只有10个miRNA在关联分析中达到显著水平（q <0.05），上调表达4个、下调表达6个。关联分析结果表明，6个下调miRNA对20个上调差异表达基因具有调控作用；4个上调miRNA对20个下调表达差异基因具有调控作用。
综上所述，本研究从miRNA和mRNA两个水平系统研究了两个品种猪骨骼肌差异表达基因，并对这些差异表达基因进行了功能注释、通路分析及互作网络调控分析等；并采用qRT-PCR方法验证了部分差异基因的表达水平。为研究不同表型猪的比较转录组学提供了宝贵的遗传资源与材料，并且有助于提高对猪转录组遗传结构的认识和理解。
The domestic pig is not only an important agricultural animal used as a source of meatworldwide, but also considered as a suitable model organism for biomedical research. Due tothe difference of genteic background and artificial selection between the Chinese indigenouspigs and foreigin commercial pig breeds, there have different intrinsic features. For instance,Laiwu pig is a typical Chinese indigenous pig, which has good meat quality; however, thewestern pig breeds have the faster grow performance than Chinese native pig breeds. It hasbeen proved that the differentially expressed genes are associated with the difference betweenChinese indigenous pig and western pig. Therefore, it is important to study the genome-widedifferentially expressed genes of skeletal muscle between Chinese native pig and western pigbreeds, and to investigate the molecular mechanism of the difference.
This experiment herein is based on the contrast of porcine skeletal muscles between theslow-growing Laiwu pig (LW) breed with better meat quality and fast-growing Yorkshire pig(YS) breed with poor meat quality. The RNA-seq technology was used to identify thedifferentially expressed miRNAs and genes of the skeletal muscle, longissimus dorsi muscle,for LW and YS pig breeds, and the identified differentially expressed miRNAs and geneswere enriched to the GO terms and KEGG pathways, which can analyze the functions of thedifferentially expressed genes. We also predicted the target genes of the differentiallyexpressed miRNAs, and constructed the regulated network between miRNAs and target genes.The miRNAs and genes expression results of the RNA-seq data were validated by the qRT-PCR, and the result shows the RNA-seq was more reliable. The results of our study arefollowing:
(1) Small RNA sequencing of longissimus dorsi muscle between LW and YS pig breeds
On average, we obtained approximately13,493,607clean reads in Laiwu pig and12,938,257clean reads in Yorkshire pig in this study. Totally,265known miRNAs wereidentified, and among these,229miRNAs were expressed in all the six pigs. In addition,94novel mature miRNAs and95novel hairpins were detected in the muscle libraries. From the265known miRNAs and95novel miRNAs,25of these miRNAs were found significantlydifferentially expressed (q <0.05). Of these significantly expressed miRNAs,10miRNAs were significantly up-regulated and15miRNAs were down-regulated in Laiwu pig comparedwith Yorkshire pig; and ssc-miR-1was the most abundant miRNA in both two pig breeds.Among the significantly expressed miRNAs, ssc-miR-194b-5p has the largest fold-change(6.35-fold). Sixteen differentially expressed miRNAs selected from high throughputsequencing were confirmed by real-time RT-PCR, and the results indicated that theexpression patterns were consistent with sequencing results. Further analysis of gene ontologyand KEGG pathway showed that249pathways were enriched which involved4,972targetgenes.
(2) Transcriptome analysis of longissimus dorsi muscle between LW and YS pig breeds
RNA-seq was applied to sample transcripts of the longissimus dorsi muscle between thetwo pig breeds to gain insights into whole-genome transcription profiles in this study. Theresulting data set provided expression patterns for many annotated, predicted and novel piggenes. We found that alternative5' first exon was the commonest type of alternative splicingevent in this study. Moreover,178significantly differentially expressed genes (q <0.05) wereidentified between the Laiwu and Yorkshire pigs, with98up-regulated and80down-regulated genes in Laiwu pig compared with Yorkshire pig. Gene expression results of theRNA-seq data were validated by qRT-PCR for twelve genes, revealing a strong correlationbetween the qRT-PCR and RNA-seq data (R2=0.93). In addition, pathway analysis revealedthat the differentially expressed genes played roles in metabolic processes, signalingpathways, and biological functions.
(3) Correlation analysis of differentially expressed miRNAs and genes
In order to investigate the functions of the differentially expressed miRNAs and genes,we analyzed the correlations of the miRNAs and genes. The results show that10miRNAwere significantly expressed between LW and YS pig breeds (q <0.05). There were4up-regulated miRNAs and6down-regulated miRNAs. The correlation results suggested that the6down-regulated miRNAs could regulate20up-regulated differentially expressed genes, andthe4up-regulated miRNAs also could regulate20down-regulated differentially expressedgenes.
In conclusion, the present study provides a comprehensive view of differences in themuscle miRNAome and transcriptome between two pig phenotypes. These results not onlycontribute to the understanding of the porcine miRNA transcriptome profiles andtranscriptome but also provide a valuable resource for future pig breeding research.
本研究选用生长速度慢但肉质优良的莱芜猪（Laiwu pig, LW）和生长速度快但肉质较差的大白猪（Yorkshire, YS）作为试验动物，利用高通量测序技术分析了莱芜猪与大白猪骨骼肌中的差异表达miRNA与差异表达基因，并对差异表达miRNA与基因进行筛选及信号通路富集，分析差异miRNA与差异基因在中外猪种中的功能。对于差异表达miRNA，采用生物信息学软件预测了这些miRNA可能的靶基因，构建了差异表达miRNA的调控网络图。为了验证高通量测序结果的正确性，我们采用qRT-PCR方法对差异表达miRNA与差异基因进行了定量验证，结果表明，高通量测序结果比较可靠。本研究的主要结果如下：
（1）莱芜猪与大白猪骨骼肌小RNA测序分析
分别构建了3个莱芜猪与3个大白猪的背最长肌小RNA文库，并利用RNA-seq技术对6个小RNA文库进行了测序，分析miRNA在莱芜猪与大白猪中的表达模式。结果表明，平均在每个莱芜猪的小RNA文库中获得了13,493,607的纯净测序reads，大白猪约为12,938,257。总共筛选出265个已知miRNA，其中有229个在6个文库中都表达；另外，还预测到94个新miRNA。对筛选出的359个miRNA进行表达分析，结果发现ssc-miR-1在两个品种猪中都是表达量最高的，而ssc-miR-194b-5p在两个品种猪中的差异倍数最大（6.35倍）；此外，还发现有25个miRNA在莱芜猪与大白猪骨骼肌中是显著差异表达（q <0.05）。在25个差异显著的miRNA中，有10个miRNA在莱芜猪中上调表达，15个下调表达。为了验证测序结果的准确性，随机选取了16个miRNA进行qRT-PCR验证，qRT-PCR结果与测序结果基本一致。对差异表达miRNA的靶基因进行预测，结果获得了10,806个靶基因，而这些靶基因主要被富集到代谢过程等信号通路中。
（2）莱芜猪与大白猪骨骼肌mRNA转录组测序分析
为了研究莱芜猪与大白猪骨骼肌全基因组的转录谱，利用RNA-seq技术对构建的两个品种猪骨骼肌文库进行测序，测序结果显示在莱芜猪的文库中获得了40,498,476的测序reads，大白猪为59,072,892；其中，80%以上的测序reads可以比对到猪的基因组中。在两个文库中共检测到12种选择性剪切类型分析，其中以TSS（转录起始位点）与TTS（转录终止位点）两种剪切类型所占的比例最大，分别占到43%和40%以上。通过对测序reads进行比对分析，结果显示在莱芜猪与大白猪骨骼肌中有10,482个共表达基因，另有739个基因只在莱芜猪中表达，712个基因只在大白猪中表达。在两个品种猪中总共预测得到1,678个新基因，其中对应2,229个新转录本。为了更进一步研究这些差异基因的功能，对这些差异基因进行检验分析，结果表明在莱芜猪与大白猪骨骼肌中有178个显著差异表达的基因（q <0.05），其中，相对于大白猪，在莱芜猪中有98个差异基因为上调表达，80个下调表达。为了验证这些差异基因的正确性，随机选取了12个差异表达基因进行qRT-PCR验证，测序结果与qRT-PCR结果基本一致，两者具有很强的相关性（R2=0.93）。对差异表达基因进行功能注释，发现差异表达基因主要被富集到代谢通路，尤其是与脂肪代谢相关的信号通路，比如脂肪酸合成代谢通路等。
（3）骨骼肌差异miRNA与差异基因关联分析
为了从整个转录水平了解两个品种猪差异表达miRNA及差异基因的功能，对178个差异表达基因与25个差异表达miRNA进行关联分析，结果表明只有10个miRNA在关联分析中达到显著水平（q <0.05），上调表达4个、下调表达6个。关联分析结果表明，6个下调miRNA对20个上调差异表达基因具有调控作用；4个上调miRNA对20个下调表达差异基因具有调控作用。
综上所述，本研究从miRNA和mRNA两个水平系统研究了两个品种猪骨骼肌差异表达基因，并对这些差异表达基因进行了功能注释、通路分析及互作网络调控分析等；并采用qRT-PCR方法验证了部分差异基因的表达水平。为研究不同表型猪的比较转录组学提供了宝贵的遗传资源与材料，并且有助于提高对猪转录组遗传结构的认识和理解。
The domestic pig is not only an important agricultural animal used as a source of meatworldwide, but also considered as a suitable model organism for biomedical research. Due tothe difference of genteic background and artificial selection between the Chinese indigenouspigs and foreigin commercial pig breeds, there have different intrinsic features. For instance,Laiwu pig is a typical Chinese indigenous pig, which has good meat quality; however, thewestern pig breeds have the faster grow performance than Chinese native pig breeds. It hasbeen proved that the differentially expressed genes are associated with the difference betweenChinese indigenous pig and western pig. Therefore, it is important to study the genome-widedifferentially expressed genes of skeletal muscle between Chinese native pig and western pigbreeds, and to investigate the molecular mechanism of the difference.
This experiment herein is based on the contrast of porcine skeletal muscles between theslow-growing Laiwu pig (LW) breed with better meat quality and fast-growing Yorkshire pig(YS) breed with poor meat quality. The RNA-seq technology was used to identify thedifferentially expressed miRNAs and genes of the skeletal muscle, longissimus dorsi muscle,for LW and YS pig breeds, and the identified differentially expressed miRNAs and geneswere enriched to the GO terms and KEGG pathways, which can analyze the functions of thedifferentially expressed genes. We also predicted the target genes of the differentiallyexpressed miRNAs, and constructed the regulated network between miRNAs and target genes.The miRNAs and genes expression results of the RNA-seq data were validated by the qRT-PCR, and the result shows the RNA-seq was more reliable. The results of our study arefollowing:
(1) Small RNA sequencing of longissimus dorsi muscle between LW and YS pig breeds
On average, we obtained approximately13,493,607clean reads in Laiwu pig and12,938,257clean reads in Yorkshire pig in this study. Totally,265known miRNAs wereidentified, and among these,229miRNAs were expressed in all the six pigs. In addition,94novel mature miRNAs and95novel hairpins were detected in the muscle libraries. From the265known miRNAs and95novel miRNAs,25of these miRNAs were found significantlydifferentially expressed (q <0.05). Of these significantly expressed miRNAs,10miRNAs were significantly up-regulated and15miRNAs were down-regulated in Laiwu pig comparedwith Yorkshire pig; and ssc-miR-1was the most abundant miRNA in both two pig breeds.Among the significantly expressed miRNAs, ssc-miR-194b-5p has the largest fold-change(6.35-fold). Sixteen differentially expressed miRNAs selected from high throughputsequencing were confirmed by real-time RT-PCR, and the results indicated that theexpression patterns were consistent with sequencing results. Further analysis of gene ontologyand KEGG pathway showed that249pathways were enriched which involved4,972targetgenes.
(2) Transcriptome analysis of longissimus dorsi muscle between LW and YS pig breeds
RNA-seq was applied to sample transcripts of the longissimus dorsi muscle between thetwo pig breeds to gain insights into whole-genome transcription profiles in this study. Theresulting data set provided expression patterns for many annotated, predicted and novel piggenes. We found that alternative5' first exon was the commonest type of alternative splicingevent in this study. Moreover,178significantly differentially expressed genes (q <0.05) wereidentified between the Laiwu and Yorkshire pigs, with98up-regulated and80down-regulated genes in Laiwu pig compared with Yorkshire pig. Gene expression results of theRNA-seq data were validated by qRT-PCR for twelve genes, revealing a strong correlationbetween the qRT-PCR and RNA-seq data (R2=0.93). In addition, pathway analysis revealedthat the differentially expressed genes played roles in metabolic processes, signalingpathways, and biological functions.
(3) Correlation analysis of differentially expressed miRNAs and genes
In order to investigate the functions of the differentially expressed miRNAs and genes,we analyzed the correlations of the miRNAs and genes. The results show that10miRNAwere significantly expressed between LW and YS pig breeds (q <0.05). There were4up-regulated miRNAs and6down-regulated miRNAs. The correlation results suggested that the6down-regulated miRNAs could regulate20up-regulated differentially expressed genes, andthe4up-regulated miRNAs also could regulate20down-regulated differentially expressedgenes.
In conclusion, the present study provides a comprehensive view of differences in themuscle miRNAome and transcriptome between two pig phenotypes. These results not onlycontribute to the understanding of the porcine miRNA transcriptome profiles andtranscriptome but also provide a valuable resource for future pig breeding research.
引文
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