Indian Journal of Animal Research

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Review Article

Latest Progress in Research on lncRNAs in Bovine Transcriptomes: A Review

Zhiqiang Han1, Hongliang Zhang1, Haiyan Zhang1, Meimei Zhu1, Wenjie Chen2, Qun Wei3, Hongxi Xu1,2,*
1Heilongjiang Academy of Agricultural Sciences, Harbin 150038, Heilongjiang, China.
2Wenzhou Vocational College of Science and Technology, Wenzhou 325006, Zhejiang, China.
3Keqiao District Animal Husbandry and Veterinary Medicine Institute, Shaoxing 312030, Zhejiang, China.

ABSTRACT

With the increasing development of deep sequencing techniques and bioinformatics tools, a large number of functional lncRNAs have been discovered. In this paper, a search of the NCBI PubMed and NCKI databases was conducted to select the functional genes that regulate muscle, fat, reproduction and immunity from the research literature of the past 5 years. The paper provides a comprehensive review of the latest research progress on the regulatory effects of lncRNAs in the transcriptomes of muscle, fat, reproduction and disease resistance, which are the key traits for improving the economic performance of the dairy and beef cattle industries.

INTRODUCTION

Long non-coding RNA (lncRNA) is a class of non-coding RNAs longer than 200 nucleotides that are produced in large quantities during the transcription of protein-coding genes. Although lncRNAs do not have protein-coding capacity, they can influence gene expression through transcriptional regulation, post-transcriptional regulation and epigenetic modifications, thereby affecting trait phenotype (Yang et al., 2021) With the development of RNA-Seq technology for transcriptome sequencing, researchers can analyse and study the structure and function of RNA at a deeper level, revealing the relationship between differentially expressed genes and organisms (Wang et al., 2017). In modern livestock production, research into the quality and yield of meat, milk and other by-products and into enhancing the regulatory role of immune factors, cytokines and other disease-fighting factors is particularly important for improving animal health, reproductive efficiency, economic benefits, animal welfare and public health (Chang et al., 2021).

lncRNAs in bovine muscle and fat transcriptome

Beef is mainly composed of muscle and fat and it is important to explore the key genes that regulate muscle and fat production in cattle to improve beef quality traits. lncRNAs regulate muscle and adipocyte differentiation in bovine their genesis, growth and development.

lncRNAs in the bovine muscle transcriptome

Beef muscle quality was assessed by the marbling of the longest dorsal muscle cross-section at the 12th to 13th sternal ribs in the same part of the carcass after cooling and acid removal and the physiological maturity of the cattle as the main assessment index. The transcriptome expression profiles of the longest dorsal muscle of yak crossbred cattle and yak showed 791 lncRNAs were differentially expressed and the lncRNA-targeted genes were significantly enriched in the HIF-1 pathway and the PI3K-Akt pathway, pathways related to myoblast differentiation and development (Huang et al., 2021). A novel lncRNA in the nucleus is highly expressed in myoblasts lnc23 is differentially expressed at different stages of embryonic development and myoblast differentiation. lnc23 is involved in key processes of myoblast differentiation, such as cell fusion and lnc23 may inhibit myoblast differentiation by decreasing cell-to-cell and cell fusion. lnc23 is a binding protein of PFN1, which is a binding protein of lnc23. lnc23 promotes myoblast differentiation by binding to PFN1 to reduce the inhibitory effect of PFN1 on RhoA and Rac1 and promoting the expression of RhoA and Rac1 proteins (Chen et al., 2021). In the genome-wide identification and analysis of lncRNAs in the dorsal longest muscle tissues of Kazakh and Xinjiang brown cattle, 182 lncRNA transcripts were found to be differentially expressed between Kazakh and Xinjiang brown cattle, of which 102 were up-regulated and 80 were down-regulated and the differentially expressed lncRNAs were associated with mitogen-activated protein kinase, Ras and phosphatidylinositol 3-kinase (PI3k)/ Akt signalling pathway (Yan et al., 2021). (Yan et al., 2021) identified a novel LncPRRX1 highly expressed in muscle tissues. LncPRRX1 promotes the proliferation of bovine myoblasts by regulating the miRNA-137/CDC42 axis (Zhang et al., 2022). Yaoyao Ma (Ma et al., 2023) screened for expression of enriched lncRNAs in bovine muscle tissues. Real-time fluorescence quantitative PCR identified 33 differentially expressed lncRNAs in different bovine tissues and screened one LncRNA13 that had an impact on bovine muscle development, named it LncRNA 5.8S rRNA-OT1 and cloned and constructed its overexpression vector pcDNA3.1-LncRNA 5.8S rRNA-OT1 (Ma et al., 2023). A novel lncRNA insulin-like growth factor 2 antisense transcript promotes proliferation and differentiation of bovine myoblasts (Song et al., 2020). The mRNA and lncRNA expression profiling at the stage of cell proliferation and differentiation in buffalo myoblasts revealed a total of 4820 differentially expressed genes, 12,227 mRNAs and 1352 lncRNAs, which were enriched in important biological processes such as the cell cycle, the p53 pathway, RNA transporter and calcium signalling pathway (Zhang et al., 2021).

lncRNAs in the bovine fat transcriptome

Bovine intramuscular fat deposition is a key indicator of the grade of marbling in the cross-section of the longest dorsal muscle. Intramuscular preadipocyte differentiation plays a key role in intramuscular fat deposition. The whole transcriptome of Qinchuan cattle intramuscular adipocytes was sequenced and analysed for mRNAs, circRNAs, lncRNAs and miRNAs at different different stages of differentiation and 31 potential key genes were identified during intramuscular preadipocyte differentiation, which included genes as shown in Table 1 and provided novel molecular breeding of beef cattle with new These genes are included in Table 1, providing new candidate marker genes for molecular breeding of beef cattle (Yang et al., 2022).

Table 1: Transcriptome lncRNA-related functional genes identified in beef tissues.



Among the lncRNAs associated with intramuscular preadipocyte differentiation and lipid deposition in yak, the lncFAM200B gene exists, which regulates the process of preadipocyte differentiation in lncFAM200B yaks (Ran et al., 2022). A 12 bp insertion/deletion (indel) variant (rs72034 3880) site was detected in the promoter region of the adipose tissue-specific lncRNA gene associated with carcass traits in cattle (Zhang et al., 2022). High-end marbled beef from Nellore cattle lncRNA 3191.1 partially overlaps with exons of the ITGAL gene and lncRNA 512.1, lncRNA 3721.1 and lncRNA 41.4 partially overlap with introns of the KRAS and MASP1 genes. kRAS and ITGAL genes are enriched in the integrin-signalling pathway associated with the pathway, marbling trait-related lncRNAs associated with calcium binding, muscle hypertrophy, skeletal muscle, adiponectin and oxidative stress response pathway associated with several related genes, lncRNA region annotated QTLs identified beef tenderness genes located on chromosome tender distributed on chromosomes 14 and 25, marbling genes distributed on chromosomes 5, 8, 25 and X (Muniz et al., 2022). Subcutaneous fat deposition in dairy cows has a variety of important immune and protective effects in vivo. By integrating genomic and transcriptomic datasets, it is possible to identify key candidate genes for subcutaneous fat deposition in high-yielding dairy cows. 46 protein-coding genes were analysed as candidate genes for regulating subcutaneous fat deposition in Holstein cows in a genome-wide association analysis study, of which 6 genes, such as NID2, STARD3, UFC1, etc., are the most critical as shown in Table 1 (Zhang et al., 2023).

lncRNA in the transcriptome of bovine reproduction system

Cattle reproductive performance directly affects the economic benefits of cattle breeding and herds with excellent production performance and high breeding value often suffer from abnormal oestrus and ovulation, low pregnancy rates, long calving intervals, lactation difficulties, low calf survival rates and male sterility. The high genetic heterogeneity and feeding environment of cattle make the study of genetic mechanisms associated with fertility very difficult (Shome et al., 2021) and the development of high-throughput sequencing technology and bioinformatics has accelerated the pace of research in genetic breeding (Jia et al., 2023).

lncRNA in the transcriptome of the bull reproductive system

Under the large-scale breeding mode, the production performance of bulls is directly related to the economic benefits of the whole cattle farm and is a key factor affecting the genetic quality of the herd. There are more and more research reports on lncRNAs related to male reproduction. Studies have shown that 10 lncRNA genes are associated with sexual maturation and spermatogenesis in bulls (Liu et al., 2021). The function of lncRNA regulation in the transcriptome of bulls can provide insight into the genetic mechanism of male sterility in Pian cattle. RNA-seq and bioinformatics analyses were used to determine the expression profiles of lncRNAs in bovine and yak testes. testicular lncRNAs NONBTAT012170 and NONBTAT010258 from different yak individuals showed high similarity and the down-regulation of the target genes of these genes during the S phase of the mitotic cell cycle resulted in abnormal DNA replication and spermatogenic blockage (Cai et al., 2021). The lncRNA and mRNA differential gene assays in PY and Yak, DEFB124, DEFB126, DEFB125 and 10 other genes are shown in Table 2, which are downregulated and involved in immune response and spermatogonial maturation (Zhao et al., 2021).

Table 2: Transcriptome lncRNA-related functional genes identified in the bovine reproductive system.



up-regulation of target genes of genes such as IGF1 and VGLL3 in lncRNAs may be related to disorders of spermatogonial maturation and cellular proliferation (Zhao et al., 2021). lncRNAs are involved in the regulation of testicular development and spermatogenesis in Holstein cows. 8-week-old calves and 80-week-old adult bulls were subjected to testicular developmental whole-transcriptome analysis and further Hub analyses yielded six lncRNAs, which regulated 71 mRNAs enriched in the testes of adult bulls, forming LncRNA-mRNA functional pairs. adult bulls were subjected to testicular cell cycle regulation, spindle assembly and sister chromatid segregation and had higher spermatogenesis than 8-week-old young bulls (Zhao et al., 2022). From the presence of lncRNA and mRNA differential expression in high and low sperm motility in the semen of Holstein bulls, the lncRNA target node gene EFNA1 is a functional gene for reproduction in bulls (Wang et al., 2019).

lncRNAs in the transcriptome of the bovine reproductive system and early embryo

Bovine oocyte growth is supported by the mutual exchange of growth signals and growth factors between granulosa cells and oocytes around its cell membrane, which support oocyte growth and regulate meiotic progression and the overall transcriptional activity of the oocyte to gain maturation capacity. mature oocyte combines with sperm to fertilise the early embryo and lncRNAs in the transcriptome of the oocyte are involved in cell adhesion, cellular differentiation, development, cell proliferation, embryonic development, signal transduction, apoptosis and aromatic compound biosynthesis (Zhao et al., 2022). lncRNAs are involved in the regulation of many key signalling pathways during oocyte maturation from the germinal ves icle stage to the mid-meiotic stage and the particularly abundant lncRNA MSTRG.19140 gene mediates oocyte meiotic resumption, progesterone-mediated oocyte maturation and cell cycle regulation (Li et al., 2021). Apoptosis and autophagy in granulosa cells surrounding oocytes are highly correlated with follicular development and atresia and LncRNA MEG3, miR-23a and apoptosis signal-regulated kinase 1 (ASK-1) are associated with it. Up-regulation of LncRNA MEG3 expression inhibited granulosa cell autophagy and promoted apoptosis and the presence of FSH or LH in yak granulosa cells reversed the effect of LncRNA MEG3 on the level of miR-23a. miR-23a levels as well as ASK1/JNK axis-mediated apoptosis and autophagy(Han et al., 2023). The X-inactivation specific transcript (XIST) of LncRNA mediates the inflammatory response in bovine mammary epithelial cells through the NF-kB/NLRP3 inflammasome pathway (Ma et al., 2019) and the XIST gene is also a major regulator of X-chromosome inactivation in the early stages of bovine embryonic development (Jali et al., 2023). During the bovine embryo transfer process embryos hatch and implant into the maternal endometrium around the time of implantation stage, blastocysts hatch and implant into the endometrial cells of the mother and endometrial extracellular vesicles (EVs) contain miRNAs and lncRNAs, which regulate physiological events, such as the epithelial-mesenchymal transition (EMT) and trophectodermal cell fusion and play a key role in the establishment of the physiological environment of the uterus (Imakawa et al., 2022). Bovine oocytes were vitrified and frozen at the germinal vesicle (GV) stage and freezing temperature and cryoprotectant concentration affected oocyte transcriptome lncRNA activity and expression and deep sequencing yielded 14 differentially expressed target genes corresponding to 17 differentially expressed lncRNAs (Mengdan Cai et al., 2022).

lncRNAs in bovine disease resistance transcriptome

Bovine nutrition, breeding environment and autoimmunity are key factors affecting bovine health, which is influenced by lncRNAs and corresponding regulatory target genes in the bovine transcriptome. Extracellular vesicles in colostrum consumed by newborn calves contain regulatory target sites of lncRNA genes that are relevant to their immune and healthy developmental functions (Shome et al., 2021). lncRNA-LRTN4RL1-AS regulates milk fat synthesis in mammary epithelial cells of dairy cows by competitively binding to miR-27a-3p to regulate PPARã expression (Jia et al., 2023).

lncRNAs in the transcriptome of bovine nutritional diseases

Nutritional levels in cattle are related to feed formulation and feeding procedures and there are many differences in metabolic efficiency and meat quality between grass- and grain-fed beef cattle, mainly caused by changes in gene expression of metabolic pathways and changes in hepatic metabolite content mediated by lncRNAs, miRNAs and ceRNAs (Jia et al., 2021). Subacute rumen acidosis (SARA) due to high concentrate ration excess is a common metabolic disease in dairy farming and differentially expressed lncRNA target genes were associated with proteasome, peroxisome and hypoxia-inducible factor-1 signalling pathways by KEGG pathway analysis (Chen et al., 2021). lncRNAs have a role in energy and lipid metabolism, the urea and tricarboxylic acid cycles and gluconeogenesis regulatory roles, especially in the regulation of lipid metabolism by fibroblast growth factor 21 (FGF21) secreted by the liver there are a large number of differentially expressed related lncRNA genes (Nolte et al., 2022).

lncRNAs in the transcriptome of bovine environmental adaptation

Organisms’ adaptation to the environment is the result of their long-term survival and development and yaks, which have been settled for a long time and widely distributed in high altitude environments, can be used as an ideal natural animal research model for the adaptation of other high altitude species, including human beings. Lungs and heart are two key organs that exhibit adaptive transcriptome changes in high altitude environments and a large number of differentially expressed genes non-linear regulation in lung tissues at different altitude environments (Ge et al., 2021). In a comparison of the transcriptomes of yaks and common cattle, 4975 mRNAs, 3326 lncRNAs and 75 miRNAs were differentially expressed; a total of 756 mRNAs, 346 lncRNAs and 83 miRNAs were differentially expressed in yaks at three different altitudes  (Wang  et al., 2021). Brain tissues such as cerebrum and cerebellum, which are the most oxygen-consuming tissues of the organism in the Class Wuqi yak, Tibetan yak and Sanjiang cattle yak, were studied and 91 candidate genes related to hypoxia were screened (Huang  et al., 2019).

lncRNAs in the transcriptome of bovine immunity to pathogenic microorganisms

Studies have shown that bovine paratuberculosis, bovine viral diarrhoea, ticks, mastitis and endometritis in dairy cows are prevalent and cause huge economic losses to the global cattle industry. lncRNAs can regulate the immune response in humans and animals at three levels, namely, transcriptional, epigenetic modification and post-transcriptional and are widely involved in the pathological regulatory processes of inflammatory diseases (Li Jia et al., 2022). The complete gene regulatory network lncRNA-mRNA-TF genes associated with bovine paratuberculosis infection was constructed by deep sequencing of lncRNAs, TFs and mRNAs and functional genes associated with the pathogenesis of bovine paratuberculosis (Heidari et al., 2021). A comprehensive analysis of lncRNAs and mRNA expression profiles in the study of bovine viral diarrhoea virus infection of bovine kidney cells, lncRNAs play an important role in host-virus interactions (Gao et al., 2021). In the early stage of bovine viral diarrhoea virus infection, the level of lncRNA IALNCR in the host cells was reduced, inhibiting the expression of MAPK8 protein and promoting the expression of caspase-3 and Bcl-2 proteins and the targeting of MAPK8 to lncRNA IALNCR antagonized viral proliferation and regulated cell-autonomous apoptosis as shown in Fig 1 (Gao et al., 2022).

Fig 1: Schematic diagram of MAPK8-targeted lncRNA IALNCR binding to antagonise bovine viral diarrhoea virus proliferation while regulating cell-autonomous apoptosis.



Extracellular vesicles in bovine plasma are tick identification and prophylactic biomarkers containing various types of RNAs, including miRNAs and lncRNAs exerting regulatory functions at the post-transcriptional level and are differentially expressed between different tick-resistant groups of cattle (Abeysinghe et al., 2021). Dairy cow mastitis is an inflammatory disease caused by infection by pathogenic microorganisms, trauma or other factors. Its incidence is high and difficult to cure, causing great harm to cow health and dairy product safety. The susceptibility or resistance of individual dairy cows to mastitis is mainly determined by genetic factors and the lncRNAs that play a role in mastitis in dairy cows are shown in Table 3 (Jia et al., 2022).

Table 3: Potential transcriptome lncRNA-related functional genes identified in bovine disease resistance systems.



Endometritis is a serious infectious disease in dairy cows after parturition. mRNA, lncRNAs and miRNAs genetic genes are involved in the pathogenesis of endometritis and their functional genes are shown in Table 3 (Sheybani et al., 2021).

CONCLUSION

At present, the research of lncRNA in the production performance, reproduction, cell differentiation, disease, breeding and other aspects of ruminants such as beef cattle and dairy cattle is still in its infancy. lncRNA as a major transcriptional regulator binds to the targeted target genes and affects their expression. The use of deep sequencing technology can be studied to prevent diseases affecting major economic traits, such as the antioxidant function of the trace element selenium has a role in preventing mastitis in dairy cows and RNA sequencing technology yields lncRNA profiles, identifies Se-associated specific lncRNAs and their associated target genes, performs functional annotations and explores selenium molecular markers for the prevention of mastitis in dairy cows to provide a new way of thinking (Jing et al., 2022). However, the research on data related to milk and beef cattle breeding is still insufficient. With the increasing demand for high-end milk and meat, strengthening the breeding of high-quality milk and beef cattle and improving the economic benefits of farming, the research on the mechanism of lncRNA regulation of gene expression in high-end milk and beef cattle will surely become a hot topic.

Authers’ contributions

Hongxi Xu: Writing-Original draft preparation; Hongliang Zhang, Qun Wei, Haiyan Zhang and Meimei Zhu: Conceptualization; Wenjie Chen: Supervision.

Funding

This work was supported by Natural Science Foundation of Heilongjiang Province-Co-guided (grant no.LH2022C092) and Special Project for Wenzhou Science and Technology Specialists (grant no. X2023070).        

CONFLICT OF INTEREST

The authors declare that there is no conflict of in this research.

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