Abstract
Long non-coding RNAs (lncRNAs) play important roles in the growth and development of skeletal muscle. However, there is limited information on goats. In this study, expression profiles of lncRNAs in Longissimus dorsi muscle from Liaoning cashmere (LC) goats and Ziwuling black (ZB) goats with divergent meat yield and meat quality were compared using RNA-sequencing. Based on our previous microRNA (miRNA) and mRNA profiles obtained from the same tissues, the target genes and binding miRNAs of differentially expressed lncRNAs were obtained. Subsequently, lncRNA-mRNA interaction networks and a ceRNA network of lncRNA-miRNA-mRNA were constructed. A total of 136 differentially expressed lncRNAs were identified between the two breeds. Fifteen cis target genes and 143 trans target genes were found for differentially expressed lncRNAs, and they were enriched in muscle contraction, muscle system process, muscle cell differentiation, and p53 signaling pathway. A total of 69 lncRNA-trans target gene pairs were constructed, with close relationship with muscle development, intramuscular fat deposition, and meat tenderness. A total of 16 lncRNA-miRNA-mRNA ceRNA pairs were identified, of which some reportedly associated with skeletal muscle development and fat deposition were found. The study will provide an improved understanding of the roles of lncRNAs in caprine meat yield and meat quality.
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Data availability
The raw data of RNA-sequencing is available at the NCBI GenBank Sequence Read Archive (SRA), under accession number PRJNA675157. Other data generated or analyzed during this study are included in this article and its supplementary information files.
References
Agliano F, Rathinam VA, Medvedev AE, Vanaja SK, Vella AT (2019) Long noncoding RNAs in host-pathogen interactions. Trends Immunol 40:492–510. https://doi.org/10.1016/j.it.2019.04.001
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29. https://doi.org/10.1038/75556
Barendse W, Bunch RJ, Harrison BE (2010) The effect of variation at the retinoic acid receptor-related orphan receptor C gene on intramuscular fat percent and marbling score in Australian cattle. J Anim Sci 88:47–51. https://doi.org/10.2527/jas.2009-2178
Bean C, Facchinello N, Faulkner G, Lanfranchi G (2008) The effects of Ankrd2 alteration indicate its involvement in cell cycle regulation during muscle differentiation. BBA-Mol Cell Res 1783:1023–1035. https://doi.org/10.1016/j.bbamcr.2008.01.027
Bolado-Carrancio A, Riancho JA, Sainz J, Rodríguez-Rey JC (2014) Activation of nuclear receptor NR5A2 increases Glut4 expression and glucose metabolism in muscle cells. Biochem Bioph Res Co 446:614–619. https://doi.org/10.1016/j.bbrc.2014.03.010
Cai B, Li Z, Ma M, Wang Z, Han P, Abdalla BA, Nie Q, Zhang X (2017) LncRNA-Six1 encodes a micropeptide to activate Six1 in cis and is involved in cell proliferation and muscle growth. Front Physiol 8:230. https://doi.org/10.3389/fphys.2017.00230
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Cheng P, Lu P, Guan J, Zhou Y, Zou L, Yi X, Cheng H (2020) LncRNA KCNQ1OT1 controls cell proliferation, differentiation and apoptosis by sponging miR-326 to regulate c-Myc expression in acute myeloid leukemia. Neoplasma 67:238–248. https://doi.org/10.4149/neo_2018_181215N972
D'Agostino M, Torcinaro A, Madaro L, Marchetti L, Sileno S, Beji S, Salis C, Proietti D, Imeneo G, Capogrossi MC, De Santa F (2018) Role of miR-200c in myogenic differentiation impairment via p66Shc: implication in skeletal muscle regeneration of dystrophic mdx mice. Oxid Med Cell Longev 2018:4814696. https://doi.org/10.1155/2018/4814696
Dransfield E, Martin JF, Bauchart D, Abouelkaram S, Lepetit J, Culioli J, Jurie C, Picard B (2003) Meat quality and composition of three muscles from French cull cows and young bulls. Anim Sci 76:387–399
Gur S, Epon M, Epin S (2003) Influence of growth rate in two growth periods on intramuscular connective tissue and palatability traits of beef. Czech J Anim Sci 48:113–119
Hocquette JF, Gondret F, Baéza E, Médale F, Jurie C, Pethick DW (2010) Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers. Animal 4:303–319. https://doi.org/10.1017/S1751731109991091
Hou X, Wang L, Zhao F, Liu X, Gao H, Shi L, Yan H, Wang L, Zhang L (2021) Genome-wide expression profiling of mRNAs, lncRNAs and circRNAs in skeletal muscle of two different pig breeds. Animals 11:3169. https://doi.org/10.3390/ani11113169
Huang C, Ge F, Ma X, Dai R, Dingkao R, Zhaxi Z, Burenchao G, Bao P, Wu X, Guo X, Chu M, Yan P, Liang C (2021) Comprehensive analysis of mRNA, lncRNA, circRNA, and miRNA expression profiles and their ceRNA networks in the Longissimus dorsi muscle of cat-tle-yak and yak. Front Genet 12:772557. https://doi.org/10.3389/fgene.2021.772557
Huang CN, Liu CL, Zeng SQ, Liu CB, Si WJ, Yuan Y, Ren LX, He YM, Zhang WY, Zhang HY, Zeng Y, Han YG, Na RS, Ee GX, Huang YF (2022) Identification of differentially expressed long non-coding RNAs and messenger RNAs involved with muscle development in Dazu black goats through RNA sequencing. Anim Biotechnol 5:1–9. https://doi.org/10.1080/10495398.2021.2020804
Jin X, Wang J, Hu J, Liu X, Li S, Lu Y, Zhen H, Li M, Zhao Z, Luo Y (2021) MicroRNA-200b regulates the proliferation and differentiation of ovine preadipocytes by targeting p27 and KLF9. Animals 11:2417. https://doi.org/10.3390/ani11082417
Kemp TJ, Sadusky TJ, Simon M, Brown R, Eastwood M, Sassoon DA, Coulton GR (2001) Identification of a novel stretch-responsive skeletal muscle gene (Smpx). Genomics 72:260–271. https://doi.org/10.1006/geno.2000.6461
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317
Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349. https://doi.org/10.1093/nar/gkm391
Kopp F, Mendell JT (2018) Functional classification and experimental dissection of long noncoding RNAs. Cell 172:393–407. https://doi.org/10.1016/j.cell.2018.01.011
Krstic J, Reinisch I, Schupp M, Schulz TJ, Prokesch A (2018) P53 functions in adipose tissue metabolism and homeostasis. Int J Mol Sci 19:2622. https://doi.org/10.3390/ijms19092622
Kuang L, Lei M, Li C, Zhang X, Ren Y, Zheng J, Guo Z, Zhang C, Yang C, Mei X, Fu M, Xie X (2018) Identification of long non-coding RNAs related to skeletal muscle development in two rabbit breeds with different growth rate. Int J Mol Sci 19:2046. https://doi.org/10.3390/ijms19072046
Kunath A, Weiner J, Krause K, Rehders M, Pejkovska A, Gericke M, Biniossek ML, Dommel S, Kern M, Ribas-Latre A, Schilling O, Brix K, Stumvoll M, Klöting N, Heiker JT, Blüher M (2021) Role of Kallikrein 7 in body weight and fat mass regulation. Biomedicines 9:131. https://doi.org/10.3390/biomedicines9020131
Li CY, Li X, Liu Z, Ni W, Zhang X, Hazi W, Ma Q, Zhang Y, Cao Y, Qi J, Yao Y, Feng L, Wang D, Hou X, Yu S, Liu L, Zhang M, Hu S (2019) Identification and characterization of long non-coding RNA in prenatal and postnatal skeletal muscle of sheep. Genomics 111:133–141. https://doi.org/10.1016/j.ygeno.2018.01.009
Li H, Huang K, Wang P, Feng T, Shi D, Cui K, Luo C, Shafique L, Qian Q, Ruan J, Liu Q (2020a) Comparison of long non-coding RNA expression profiles of cattle and buffalo differing in muscle characteristics. Front Genet 11:98. https://doi.org/10.3389/fgene.2020.00098
Li J, Yang T, Tang H, Sha Z, Chen R, Chen L, Yu Y, Rowe GC, Das S, Xiao J (2021) Inhibition of lncRNA MAAT controls multiple types of muscle atrophy by cis- and trans-regulatory actions. Mol Ther 29:1102–1119. https://doi.org/10.1016/j.ymthe.2020.12.002
Li Q, Liu R, Zhao H, Di R, Lu Z, Liu E, Wang Y, Chu M, Wei C (2018) Identification and characterization of long noncoding RNAs in ovine skeletal muscle. Animals 8:127. https://doi.org/10.3390/ani8070127
Li R, Li B, Jiang A, Cao Y, Hou L, Zhang Z, Zhang X, Liu H, Kim KH, Wu W (2020b) Exploring the lncRNAs related to skeletal muscle fiber types and meat quality traits in pigs. Genes 11:883. https://doi.org/10.3390/genes11080883
Li T, Wan S, Wu R, Zhou X, Zhu D, Zhang Y (2012) Identification of long non-protein coding RNAs in chicken skeletal muscle using next generation sequencing. Genomics 99:292–298. https://doi.org/10.1016/j.ygeno.2012.02.003
Li Z, Ouyang H, Zheng M, Cai B, Han P, Abdalla BA, Nie Q, Zhang X (2017) Integrated analysis of long non-coding RNAs (lncRNAs) and mRNA expression profiles reveals the potential role of lncRNAs in skeletal muscle development of the chicken. Front Physiol 7:687. https://doi.org/10.3389/fphys.2016.00687
Ling Y, Zheng Q, Sui M, Zhu L, Xu L, Zhang Y, Liu Y, Fang F, Chu M, Ma Y, Zhang X (2019) Comprehensive analysis of lncRNA reveals the temporal-specific module of goat skeletal muscle development. Int J Mol Sci 20:3950. https://doi.org/10.3390/ijms20163950
Liu J, Zhou Y, Hu X, Yang J, Lei Q, Liu W, Han H, Li F, Cao D (2021a) Transcriptome analysis reveals the profile of long non-coding RNAs during chicken muscle development. Front Physiol 12:660370. https://doi.org/10.3389/fphys.2021.660370
Liu YX, Ma XM, Xiong L, Wu XY, Liang CN, Bao PJ, Yu QL, Yan P (2021b) Effects of intensive fattening with total mixed rations on carcass characteristics, meat quality, and meat chemical composition of yak and mechanism based on serum and transcriptomic profiles. Front Vet Sci 7:599418. https://doi.org/10.3389/fvets.2020.599418
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484. https://doi.org/10.1093/nar/gkm882
Park JW, Lee JH, Han JS, Shin SP, Park TS (2020) Muscle differentiation induced by p53 signaling pathway-related genes in myostatin-knockout quail myoblasts. Mol Biol Rep 47:9531–9540. https://doi.org/10.1007/s11033-020-05935-0
Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290–295. https://doi.org/10.1038/nbt.3122
Quan J, Kang Y, Luo Z, Zhao G, Liu Z (2021) Integrated analysis of the responses of a circRNA-miRNA-mRNA ceRNA network to heat stress in rainbow trout (Oncorhynchus mykiss) liver. BMC Genomics 22:48. https://doi.org/10.1186/s12864-020-07335-x
Ren C, Deng M, Fan Y, Yang H, Zhang G, Feng X, Li F, Dan W, Wang F, Zhang Y (2017) Genome-Wide analysis reveals extensive changes in LncRNAs during skeletal muscle development in Hu Sheep. Genes 8:191. https://doi.org/10.3390/genes8080191
Ronzoni FL, Giarratana N, Crippa S, Quattrocelli M, Cassano M, Ceccarelli G, Benedetti L, Van Herck J, Cusella De Angelis MG, Vitale M, Galli D, Sampaolesi M (2021) Guide cells support muscle regeneration and affect Neuro-Muscular junction organization. Int J Mol Sci 22:1939. https://doi.org/10.3390/ijms22041939
Rosa AF, Moncau CT, Poleti MD, Fonseca LD, Balieiro JCC, Silva SLE, Eler JP (2017) Proteome changes of beef in Nellore cattle with different genotypes for tenderness. Meat Sci 138:1. https://doi.org/10.1016/j.meatsci.2017.12.006
Sheela SG, Lee WC, Lin WW, Chung BC (2005) Zebrafish ftz-f1a (nuclear receptor 5a2) functions in skeletal muscle organization. Dev Biol 286:377–390. https://doi.org/10.1016/j.ydbio.2005.06.023
Shen J, Hao Z, Luo Y, Zhen H, Liu Y, Wang J, Hu J, Liu X, Li S, Zhao Z, Liu Y, Yang S, Wang L (2022b) Deep small RNA sequencing reveals important mirnas related to muscle development and intramuscular fat deposition in Longissimus dorsi muscle from different goat breeds. Front Vet Sci 9:911166. https://doi.org/10.3389/fvets.2022.911166
Shen J, Hao Z, Wang J, Hu J, Liu X, Li S, Ke N, Song Y, Lu Y, Hu L, Qiao L, Wu X, Luo Y (2021) Comparative transcriptome profile analysis of Longissimus dorsi muscle tissues from two goat breeds with different meat production performance using RNA-Seq. Front Genet 11:619399. https://doi.org/10.3389/fgene.2020.619399
Shen J, Zhen H, Li L, Zhang Y, Wang J, Hu J, Liu X, Li S, Hao Z, Li M, Zhao Z, Luo Y (2022a) Identification and characterization of circular RNAs in Longissimus dorsi muscle tissue from two goat breeds using RNA-Seq. Mol Genet Genomics 297:817–831. https://doi.org/10.1007/s00438-022-01887-1
Shi T, Hu W, Hou H, Zhao Z, Shang M, Zhang L (2020) Identification and comparative analysis of long non-coding RNA in the skeletal muscle of two dezhou donkey strains. Genes 11:508. https://doi.org/10.3390/genes11050508
Sun L, Luo H, Bu D, Zhao G, Yu K, Zhang C, Liu Y, Chen R, Zhao Y (2013) Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res 41:e166. https://doi.org/10.1093/nar/gkt646
Teixeira A, Silva S, Rodrigues S (2019) Advances in sheep and goat meat products research. Adv Food Nutr Res 87:305–370. https://doi.org/10.1016/bs.afnr.2018.09.002
Tsai SH, Chang EY, Chang YC, Hee SW, Tsai YC, Chang TJ, Chuang LM (2013) Knockdown of RYR3 enhances adi-ponectin expression through an ATF3-dependent pathway. Endocrinology 154:1117–1129. https://doi.org/10.1210/en.2012-1515
Wang J, Ren Q, Hua L, Chen J, Zhang J, Bai H, Li H, Xu B, Shi Z, Cao H, Xing B, Bai X (2019) Comprehensive analysis of differentially expressed mRNA, lncRNA and circRNA and their ceRNA networks in the Longissimus dorsi muscle of two different pig breeds. Int J Mol Sci 20:1107. https://doi.org/10.3390/ijms20051107
Wang JQ, Shen JY, Liu X, Li SB, Luo YZ, Zhao ML, Hao ZY, Ke N, Song YZ, Qiao LQ (2021) Comparative analysis of meat production traits, meat quality, and muscle nutrient and fatty acid contents between Ziwuling black goats and Liaoning cashmere goats. Acta Pratacul Sin 30:166–177. https://doi.org/10.11686/cyxb2020199
Wang YN, Yang WC, Li PW, Wang HB, Zhang YY, Zan LS (2018) Myocyte enhancer factor 2A promotes proliferation and its inhibition attenuates myogenic differentiation via myozenin 2 in bovine skeletal muscle myoblast. PloS One 13:e0196255. https://doi.org/10.1371/journal.pone.0196255
Yan XM, Zhang Z, Liu JB, Li N, Yang GW, Luo D, Zhang Y, Yuan B, Jiang H, Zhang JB (2021) Genome-wide identification and analysis of long noncoding RNAs in longissimus muscle tissue from Kazakh cattle and Xinjiang brown cattle. Anim Biosci 34:1739–1748. https://doi.org/10.5713/ajas.20.0317
Yao CX, Wei QX, Zhang YY, Wang WP, Xue LX, Yang F, Zhang SF, Xiong CJ, Li WY, Wei ZR, Zou Y, Zang MX (2013) MiR-200b targets GATA-4 during cell growth and differentiation. RNA Biol 10:465–480. https://doi.org/10.4161/rna.24370
Yao RW, Wang Y, Chen LL (2019) Cellular functions of long noncoding RNAs. Nat Cell Biol 21:542–551. https://doi.org/10.1038/s41556-019-0311-8
Zhan S, Dong Y, Zhao W, Guo J, Zhong T, Wang L, Li L, Zhang H (2016) Genome-wide identification and characterization of long non-coding RNAs in developmental skeletal muscle of fetal goat. BMC Genomics 17:666. https://doi.org/10.1186/s12864-016-3009-3
Zhan S, Qin C, Li D, Zhao W, Nie L, Cao J, Guo J, Zhong T, Wang L, Li L, Zhang H (2019) A novel long noncoding RNA, lncR-125b, promotes the differentiation of goat skeletal muscle satellite cells by sponging miR-125b. Front Genet 10:1171. https://doi.org/10.3389/fgene.2019.01171
Zhu S, Chen CY, Hao Y (2021) LncRNA KCNQ1OT1 acts as miR-216b-5p sponge to promote colorectal cancer progression via up-regulating ZNF146. J Mol Histol 52:479–490. https://doi.org/10.1007/s10735-020-09942-0
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This research was funded by the Fuxi Young Talent Fund of Gansu Agricultural University (Gaufx-02Y02), the Science and Technology project of Lanzhou city (2021-1-162), the Central Guidance on Local Science and Technology Development Fund of Gansu Province, Lanzhou City Overseas Expertise Introduction Base for Molecular Breeding of Mutton Sheep, the Projects of Gansu Agricultural University (GSAU-ZL-2015-033), and Discipline Team Project of Gansu Agricultural University (GAU-XKTD-2022-21).
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Jiyuan Shen and Jiqing Wang conceived and designed the experiments; Jiyuan Shen, Yuzhu Luo, Jiang Hu, Xiu Liu, and Shaobin Li conducted the experiments; Zhiyun Hao, Mingna Li, Zhidong Zhao, Yuting Zhang, Shutong Yang, Longbin Wang, and Yuanhua Gu analyzed the data; Jiyuan Shen and Jiqing Wang drafted and revised the manuscript. All authors read and approved the final manuscript.
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All animal procedures in this study were approved by the Animal Experiment Ethics Committee of Gansu Agricultural University with an approval number of GSAU-ETH-AST-2021-028.
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Shen, J., Luo, Y., Wang, J. et al. Integrated transcriptome analysis reveals roles of long non-coding RNAs (lncRNAs) in caprine skeletal muscle mass and meat quality. Funct Integr Genomics 23, 63 (2023). https://doi.org/10.1007/s10142-023-00987-4
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DOI: https://doi.org/10.1007/s10142-023-00987-4