肉牛大理石花纹等级相关lncRNA筛选与特征分析

doi:10.7668/hbnxb.20193934

摘要/Abstract

摘要：

牛肉大理石花纹特征是由多基因调控的重要肉质性状,是衡量高档牛肉品质的条件之一。LncRNA是一种重要的非编码RNA,在调节脂肪沉积的相关生物学过程中发挥重要作用。为了解lncRNA在肉牛不同大理石花纹表型中的潜在生物学作用,采集高(A5)、低(A1)2种极端等级大理石花纹的杂交和牛背最长肌组织,利用高通量测序方法检测与肉质大理石花纹相关的差异lncRNA,预测差异lncRNA反式作用靶基因,并对其进行功能富集分析。结果表明,在2个等级大理石花纹牛肉组织中共筛选出45个显著差异lncRNA,其中在高等级大理石花纹组织中分别有21,24个显著上调及下调的lncRNA,包括MSTRG.9509.3、ENSBTAT00000077612、ENSBTAT00000072841等与脂肪沉积相关的lncRNA。对反式作用靶基因的功能富集分析表明,预测靶基因显著富集到脂多糖结合、脂肪分解等脂肪沉积相关的生物学过程。差异lncRNA可能通过反式作用靶向脂肪沉积相关基因(FABP4、PLIN1、LIPE等)参与调节肉牛大理石花纹表型特征。检测到的牛肉大理石花纹相关差异lncRNA、预测靶基因及其富集通路将为拓展对非编码RNA生物学功能的认识及其与牛肉大理石花纹特征的关系奠定基础,也为农业家畜的优质性状解析与新品种培育提供参考。

关键词: 肉牛, 大理石花纹, 长链非编码RNA, 肌内脂肪, 肉品质

Abstract:

Beef marbling is an important meat quality trait regulated by multiple genes and is one of the conditions to measure the quality of high grade beef.LncRNA is an important non-coding RNA that plays an important role in regulating the biological processes related to fat deposition.To understand the potential biological role of lncRNA in different marbling phenotypes in beef cattle,this study collected crossbred and the longest dorsal muscle tissues from two extreme grades of high(A5)and low(A1)marbling,and used high-throughput sequencing to detect differential lncRNA associated with meat marbling,predict the trans-acting target genes of differential lncRNA,and perform functional enrichment for the analysis.The results showed that a total of 45 significantly different lncRNA were screened in two grades of marbled beef tissues,including 21 and 24 significantly up- and down-regulated lncRNA in high-grade marbled tissues,respectively,including MSTRG.9509.3,ENSBTAT00000077612,ENSBTAT00000072841 and other lncRNA associated with lipid deposition.Functional enrichment analysis of trans-acting target genes showed that predicted target genes were significantly enriched to lipopolysaccharide binding,lipolysis and other biological processes associated with lipid deposition.Differential lncRNA may be involved in regulating beef marbling phenotypic traits by targeting fat deposition-related genes(FABP4,PLIN1,LIPE,etc.)through trans-activation.The detection of beef marbling-related differential lncRNA,predicted target genes and their enrichment pathways would provide a basis for expanding the understanding of the biological functions of non-coding RNAs and their relationship with beef marbling characteristics,as well as a reference for the analysis of quality traits and breeding of new breeds in agricultural livestock.

Key words: Beef cattle, Marbling, LncRNA, Intramuscular fat, Meat quality

曾灵, 张岩峰, 李承隆, 丁燕玲, 周小南, 明文轩, 苏总华, 曲畅, 徐俊杰, 史远刚, 康晓龙. 肉牛大理石花纹等级相关lncRNA筛选与特征分析[J]. 华北农学报, 2023, 38(S1): 371-380. doi: 10.7668/hbnxb.20193934.

ZENG Ling, ZHANG Yanfeng, LI Chenglong, DING Yanling, ZHOU Xiaonan, MING Wenxuan, SU Zonghua, QU Chang, XU Junjie, SHI Yuangang, KANG Xiaolong. Screening and Characterization of LncRNA Associated with Marbling Grade in Beef Cattle[J]. Acta Agriculturae Boreali-Sinica, 2023, 38(S1): 371-380. doi: 10.7668/hbnxb.20193934.

http://www.hbnxb.net/CN/Y2023/V38/IS1/371

图/表 10

图1 杂交和牛牛肉大理石花纹等级表型 A.大理石花纹等级为A1的肌肉组织;B.大理石花纹等级为A5的肌肉组织。

Fig.1 Marbling grade phenotypes of crossbred Wagyu cattle A.Muscle tissue with a marbling grade of A1;B.Muscle tissue with a marbling grade of A5.

表1 定量验证lncRNA的引物信息

Tab.1 Primer information of quantitative validation for lncRNA

引物名称 Primer name	引物序列(5'—3') Primer sequences(5'—3')	产物长度/bp Product length	退火温度/℃ Annealing temperature
MSTRG.9911.1	F:CCCTCTGTGCCTGCTATT	187	54.0
	R:GGTTCCCGATGTAAGTGTC
MSTRG.9509.3	F:CACCTTGGCTGGTAACGC	352	56.3
	R:GGAGGGATCTCGGATTGG
ENSBTAT00000071741	F:ACTTCCGCCTTGCTTTCAG	141	57.0
	R:CCTTCCCTCAGCGTTGGT
MSTRG.1867.3	F:GCCCTTGTGCCCTGTAGAAA	222	59.0
	R:CCAAGCCCAGTGTCAGTGTCT
ENSBTAT00000077612	F:CATAGGGACTGTCGTGATT	141	50.4
	R:TTCCGATTCTTCTGCTTT
MSTRG.2227.1	F:CCTCATTCCCTGTTGGTT	189	50.3
	R:TATTGGCACTTTGGCTTC
ENSBTAT00000079684	F:GGGTTACATAAGGATTCAAGTT	222	52.0
	R:AAGTAAGAGGTTAGGCAGGTC
ENSBTAT00000072841	F:GGGCAACGCTGAGGTCTA	158	55.0
	R:GCACGAACTCGAAACAATCT
MSTRG.9442.3	F:CCCATGAGACCAGTTGAT	419	51.3
	R:TGAAGGAAAGACAGAGGC
GAPDH	F:TCGGAGTGAACGGATTCGGC	82	54.0
	R:ATGGCGACGATGTCCACTTT

表2 测序数据质控统计分析

Tab.2 Statistical analysis of sequencing data quality control

样品 Samples	原始序列 Raw reads	纯净序列 Clean reads	纯净序列/原始序列/% Clean reads/Raw reads	Q20/%	Q30/%
A1-1	111 554 164	111 194 184	99.68	97.54	93.56
A1-2	101 269 128	100 892 594	99.63	97.22	92.88
A1-3	96 917 862	96 549 646	99.62	97.14	92.69
A5-1	90 769 326	90 410 038	99.60	97.22	93.00
A5-2	96 145 566	95 822 408	99.66	97.26	93.13
A5-3	91 064 624	90 728 852	99.63	97.39	93.25

表3 测序数据基因组比对统计

Tab.3 Sequencing data genome alignment statistics

样品 Samples	总数据/条 Total reads	比对量/条 Map reads	比对率/% Map rate	唯一比对/条 Unique mapped	唯一比对率/% Unique mapped rate
A1-1	110 637 006	104 215 448	94.20	99 466 504	89.90
A1-2	100 489 580	94 541 731	94.08	89 773 862	89.34
A1-3	95 736 800	89 862 658	93.86	84 910 423	88.69
A5-1	89 742 628	84 181 762	93.80	79 015 339	88.05
A5-2	95 508 118	89 146 832	93.34	84 419 850	88.39
A5-3	90 293 804	85 179 073	94.34	80 724 889	89.40

图2 lncRNA表达量丰度分布及新lncRNA鉴定 A.横坐标为log₁₀FPKM,该数值越高,表示基因表达量越高;纵坐标为基因的密度,即对应横轴某表达量水平的基因数;峰值表示该表达量水平的蛋白编码基因数最多;B.各样本基因表达水平小提琴图:纵轴方向宽度代表数据弥散程度,横轴方向长度代表在某纵坐标位置数据分布多少;C.CNCI和CPC2注释结果的Venn图;D.新lncRNA转录类型统计图。

Fig.2 Distribution of lncRNA expression abundance and identification of novel lncRNA A.The horizontal coordinate is log₁₀FPKM,the higher values,higher gene expression;the vertical coordinate is the density of genes,i.e.the number of genes corresponding to a certain of expression level on the horizontal axis;The peak indicates the highest number of protein-coding genes at this expression level;B.Violin plots of gene expression levels for each sample:the length of the vertical axis represents the degree of data dispersion,and the width of the horizontal axis represents the distribution of data at a given vertical coordinate position;C.Venn diagram of CNCI and CPC2 annotation;D.Statistical plot of new lncRNA transcript types.

图3 极端等级大理石花纹相关差异lncRNA的表达模式 A.A1和A5 2组中差异lncRNA数统计;B.A1和A5 2组差异lncRNA火山图:y轴为Padj的对数值,x轴为差异倍数;C.A1和A5 2组差lncRNAs的热图,每列代表一个样品,每行代表一个lncRNA;基因在不同样品中的表达量用不同颜色表示,红色表示高表达,蓝色表示低表达。

Fig.3 Expression patterns of differential lncRNA associated with extreme grades of marbling A.Statistics of the number of differential lncRNA in A1 and A5 groups;B.Differential lncRNA volcano plot:y-axis is the logarithm of Padj,x-axis is the difference multiplier;C.Heatmap of differential lncRNAs in A1 and A5 groups.Each column represents one sample,each row represents one lncRNA;genes expression in different samples are indicated by different colors,red for high expression and blue for low expression.

图4 大理石花纹相关差异lncRNA的靶基因GO功能富集 A:1.质膜部分 GO:0044459;2.细胞表面 GO:0009986;3.浆膜的外侧 GO:0009897;4.膜的一侧 GO:0098552;5.细胞外区域部分 GO:0044421;6.细胞外区域 GO:0005576;7.质膜的内在成分 GO:0031226;8.细胞周边 GO:0071944;9.浆膜 0005886;10.浆膜的整体部分 GO:0005887;11.细胞外空间 GO:0005615;12.浆膜蛋白复合物 GO:0098797;13.膜部分 GO:0044425;14.浆膜区域 GO:0098590;15.膜的内在成分 GO:0031224;16.含胶原蛋白的细胞外基质 GO:0062023;17.突触膜 GO:0097060;18.细胞外基质 GO:0031012;19.质膜受体复合体 GO:0098802;20.受体复合体 GO:0043235。B:1.跨膜转运器活性 GO:0022857;2.信号受体的结合 GO:0005102;3.转运体活性 GO:0005215;4.运动活性 GO:0003774;5.脂多糖的结合 GO:0001530;6.C-C趋势化因子受体活性 GO:0016493;7.C-C趋化因子结合 GO:0019957;8.细胞因子受体活性 GO:0004896;9.非跨膜蛋白酪氨酸激酶活性 GO:0004715;10.ATP依赖的微管马达活性 GO:1990939;11.微管运动活性 GO:0003777;12.G蛋白偶联的化合剂受体活性 GO:0001637;13.趋化因子受体活性 GO:0004950;14.雄性激素脱氢酶活性 GO:0047023;15.细胞粘附分子结合 GO:0050839;16.趋化因子活性 GO:0008009;17.单氧酶活性 GO:0004497;18.无机分子实体跨膜转运器活性 GO:0015318;19.活性跨膜转运体活性 GO:0022804;20.阳离子跨膜转运体的活性 GO:0008324。C:1.免疫系统过程 GO:0002376;2.免疫反应 GO:0006955;3.免疫系统过程的调节 GO:0002682;4.细胞激活 GO:0001775;5.对外部刺激的反应 GO:0009605;6.防御反应 GO:0006952;7.白细胞激活 GO:0045321;8.免疫系统过程的积极调节 GO:0002684;9.细胞激活的调节 GO:0050865;10.淋巴细胞的激活 GO:0046649;11.细胞表面受体信号传导途径 GO:0007166;12.对其他生物体的反应 GO:0051707;13.对外部生物刺激的反应 GO:0043207;14.对生物刺激的反应 GO:0009607;15.免疫效应器过程 GO:0002252;16.白细胞激活的调节 GO:0002694;17.生物粘附 GO:0022610;18.对刺激反应的调节 GO:0048583;19.先天免疫反应 GO:0045087;20.免疫反应的调节 GO:0050776。

Fig.4 GO functional enrichment of marbling-associated differential lncRNA for target gene A:1.Plasma membrane part;2.Cell surface;3.External side of plasma membrane;4.Side of membrane;5.Extracellular region part;6.Extracellular region;7.Intrinsic component of plasma membrane;8.Cell periphery;9.Plasma membrane;10.Integral component of plasma membrane;11.Extracellular space;12.Plasma membrane protein complex;13.Membrane part;14.Plasma membrane region;15.Intrinsic component of membrane;16.Collagen-containing extracellular matrix;17.Synaptic membrane;18.Extracellular matrix;19.Plasma membrane receptor complex;20.Receptor complex.B:1.Transmembrane transporter activity;2.Signaling receptor binding;3.Transporter activity;4.Motor activity;5.Lipopolysaccharide binding;6.C-C Chemokine receptor activity;7.C-C Chemokine binding;8.Cytokine receptor activity;9.Non-membrane spanning protein tyrosine kinase activity;10.ATP-dependent Microtubule motor activity;11.Microtubule motor activity;12.G Protein-coupled chemoattractant receptor activity;13.Chemokine receptor activity;14.Androsterone dehydrogenase activity;15.Cell adhesion molecule binding;16.Chemokine activity;17.Monooxygenase activity;18.Inorganic molecular entity transmembrane transporter activity;19.Active transmembrane transporter activity;20.Cation transmembrane transporter activity.C:1.Immune system process;2.Immune response;3.Regulation of immune system process;4.Cell activation;5.Response to external stimulus;6.Defense response;7.Leukocyte activation;8.Positive regulation of immune system process;9.Regulation of cell activation;10.Lymphocyte activation;11.Cell surface receptor signaling pathway;12.Response to other organism;13.Response to external biotic stimulus;14.Response to biotic stimulus;15.Immune effector process;16.Regulation of leukocyte activation;17.Biological adhesion;18.Regulation of response to stimulus;19.Innate immune response;20.Regulation of immune response.

图5 差异lncRNA靶基因的KEGG通路分析 1.单纯疱疹感染;2.病毒蛋白与细胞因子和细胞因子受体的相互作用;3.碱基切除修复;4.细胞因子-细胞因子受体的相互作用;5.细胞凋亡;6.细胞粘附分子(CAMs);7.长寿调节途径-蠕虫;8.趋化因子信号通路;9.卵巢类固醇生成;10.胆汁分泌;11.移植物抗宿主疾病;12.造血细胞系;13.卡波西肉瘤相关的疱疹病毒感染;14.自然杀伤细胞介导的细胞毒性;15.脂肪细胞中脂肪分解的调节;16.抗原处理和呈现;17.IL-17信号传导途径;18.Ⅰ型糖尿病;19.补体和凝血级联;20.抗逆转录病药物抵抗。

Fig.5 KEGG pathway enrichment of target gene from differential lncRNA 1.Herpes simplex infection;2.Viral protein interaction with cytokine and cytokine receptor;3.Base excision repair;4.Cytokine-cytokine receptor interaction;5.Apoptosis;6.Cell adhesion molecules(CAMs);7.Longevity regulating pathway-worm;8.Chemokine signaling pathway;9.Ovarian steroidogenesis;10.Bile secretion;11.Graft-versus-host disease;12.Hematopoietic cell lineage;13.Kaposi sarcoma-associated Herpesvirus infection;14.Natural killer cell mediated cytotoxicity;14.Regulation of lipolysis in adipocyte;16.Antigen processing and presentation;17.IL-17 Signaling pathway;18.TypeⅠ diabetes mellitus;19.Complement and coagulation cascades;20.Antifolate resistance.

图6 脂肪沉积相关lncRNA-靶基因-生物学过程的调控网络长方形.差异表达lncRNA;菱形.靶基因;三角形.与脂肪沉积相关的生物学过程;绿色.基因表达上调;红色.基因表达下调。

Fig.6 A regulatory network of fat deposition-associated lncRNA-target gene-biological processes Rectangles.Differentially expressed lncRNA;Diamonds.Target genes;Triangles.Biological processes associated with fat deposition;Green.Up-regulated gene expression;Red.Down-regulated gene expression.

图7 RNA-seq与qRT-PCR结果比较

Fig.7 Comparison of RNA-seq and qRT-PCR results

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