|
|
Effects of Early Supplementation with Starter on Rumen Tissue Transcriptome in Lambs (Ovis aries) |
WANG Xiao-Juan*, LYU Feng, PANG Xin, LIU Guo-Hua, ZHAO Hai-Bi |
College of Animal Science and Technology, Gansu Agricultural University, Lanzhou 730070, China |
|
|
Abstract Rumen is an important digestive organ of ruminants, early supplementation with starter can meet the nutritional needs of rapid growth of lambs (Ovis aries) and promote the early development of rumen. This study was conducted to investigate the effects of supplementation with starter on gene expression in rumen tissues of lambs to clarify the possible mechanism of starter on rumen development. Twenty-two healthy and disease-free male Hu lambs (birth weight=(3.65±0.49) kg) were randomly divided into 2 groups, control group and supplementary feeding group. Control group was fed with milk replacer, while supplementary feeding group was fed with milk replacer and starter. At the age of 28 days, rumen pouch tissues were collected for transcriptome sequencing analysis. The result showed that 61.70 and 58.95 Gb of clean reads were obtained in control group and supplementary feeding group, respectively, and the comparison efficiency with the reference genome was 87.85%~89.45%. Compared with the control group, 868 differentially expressed genes were screened after supplementary feeding, among which 464 genes were up-regulated and 404 genes were down-regulated. And it was mainly concentrated in GO functions such as enzyme activity, ion channel and membrane transport and KEGG signaling pathways such as steroid hormone biosynthesis, arachidonic acid metabolism, peroxisome proliferator-activated receptor (PPAR) signaling pathway, regulation of lipolysis in adipocytes and cyclic adenosine monophosphate (cAMP) signaling pathway. Correlation analysis showed that recombinant IQ motif containing GTPase activating protein 2 (IQGAP2), recombinant solute carrier family 16, member 1 (SLC16A1), ankyrin repeat domain-containing protein 45 (ANKRD45), 3-hydroxy-3-methylglutaryl-CoA, synthase 2 (HMGCS2), phosophoenolpyruvate carboxykinase 2 (PCK2) were significantly positively correlated with the length of rumen papilla, the concentration of acetate, propionate, butyrate and total volatile fatty acid (TVFA)(P<0.05), while ceramide synthase 3 (CERS3), recombinant keratin 4 (KRT4), solute carrier family 22A17 (SLC22A1), recombinant insulin like growth factor binding protein 6 (IGFBP6) were significantly negatively correlated (P<0.05). Supplementation with starter may promote rumen development by regulating the expression of genes related to rumen epithelial proliferation and nutrient generation. This study provides a basis for further exploring the mechanism of supplemental starter on rumen development.
|
Received: 26 May 2021
|
|
Corresponding Authors:
*wangxj@gsau.edu.cn
|
|
|
|
[1] 刘婷, 李发弟,王维民, 等. 2016. 不同日龄补饲开食料对湖羊羔羊瘤胃形态及表皮生长相关基因表达的影响[J]. 畜牧兽医学报, 47(12): 2441-2449. (Liu T, Li F D, Wang W M, et al.2016. Effects of starter feeding on rumen papilla genes expression involved cellular growth and morphology in Hu lamb at different ages[J]. Acta Veterinaria et Zootechnica Sinica, 47(12): 2441-2449.) [2] 马仲华. 2002. 家畜解剖学及组织胚胎学[M]. 中国农业出版社, 北京, pp. 79-95. (Ma Z H.2002. Anatomy and Histoembryology of the Domestic Animals[M]. China Agriculture Science and Technique Press, Beijing, pp. 79-95.) [3] 汪晓娟. 2015. 早期开食对羔羊瘤胃发育的影响及其机理研究[D]. 博士学位论文, 甘肃农业大学, 导师: 李发弟. pp. 69-79. (Wang X J.2015. Effect of starter feeding on development of the rumen on lambs[D]. Thesis for M.S., Gansu Agriculture University, Supervisor: Li F D, pp. 69-79.) [4] 杨斌. 2017. 早期补饲苜蓿调节幼龄湖羊生长和瘤胃发育的机制研究[D]. 博士学位论文, 浙江大学, 导师: 王佳堃, pp. 26-30. (Yang B.2017. Mechanism in growth and rumen development alteration by early alfalfa supplementation in Hu lambs[D]. Thesis for M.S., Zhejiang University, Supervisor: Wang J K, pp. 26-30.) [5] 岳喜新, 刁其玉, 马春晖, 等. 2011. 早期断奶羔羊代乳粉饲喂水平对营养物质消化代谢及血清生化指标的影响[J]. 中国农业科学, (21): 4464-4473. (Yue X X, Diao Q Y, Ma C H, et al. 2011. Effects of feeding levels of a milk replacer on digestion and metabolism of nutrients, serum biochemical indexes in lambs[J]. Scientia Agricultura Sinica, (21): 4464-4473.) [6] Aschenbach J R, Bilk S, Tadesse G, et al.2009. Bicarbonate-dependent and bicarbonate-independent mechanisms contribute to nondiffusive uptake of acetate in the ruminal epithelium of sheep[J]. American Journal of Physiology, 296(5): G1098-1107. [7] Aschenbach J R, Penner G B, Stumpff F, et al.2011. Ruminant nutrition symposium: Role of fermentation acid absorption in the regulation of ruminal pH[J]. Journal of animal science, 89(4): 1092-1107. [8] Barrick D, Ferreiro D U, Komives E A.2008. Folding landscapes of ankyrin repeat proteins: Experiments meet theory[J]. Current Opioion in Structural Biology, 18(1): 27-34. [9] Bionaz M, Loor J J.2012. Ruminant metabolic systems biology: Reconstruction and integration of transcriptome dynamics underlying functional responses of tissues to nutrition and physiological state[J]. Gene Regulation Systems Biology, 6: 109-125. [10] Deng Z, Wang L, Hou H, et al.2016. Epigenetic regulation of IQGAP2 promotes ovarian cancerprogression via activating Wnt/β -catenin signaling[J]. International Journal of Oncology, 48(1): 153-160. [11] Dias J, Marcondes M I, Noronha MF, et al.2017. Effect of pre-weaning diet on the ruminal archaeal, bacterial, and fungal communities of dairy calves[J]. Frontiers in Microbiology, 8: 1553. [12] Fisel P, Schaeffeler E, Schwab M.2018. Clinical and functional relevance of the monocarboxylate transporter family in disease pathophysiology and drug therapy[J]. Clinical and Translational Science, 11(4): 352-364. [13] Futagi Y, Kobayashi M, Narumi K, et al.2019. Homology modeling and site-directed mutagenesis identify amino acid residues underlying the substrate selection mechanism of human monocarboxylate transporters 1 (hMCT1) and 4 (hMCT4)[J]. Cellular and Molecular Life Sciences, 76(24): 4905-4921. [14] Gäbel G, Aschenbach J R, Müller F.2002. Transfer of energy substrates across the ruminal epithelium: Implications and limitations[J].Animal Health Research Reviews, 3(1): 15-30. [15] Ghaleb A M, Bialkowska A B, Snider A J, et al.2015. IQ motif-containing GTPase-activating protein (IQGAP2) is a novel regulator of colonicinflammation in mice[J]. PLOS ONE, 10(6): e0129314. [16] Heinrichs J.2005. Rumen development in the dairy calf[J]. Dairy Research Teaching and Extension, 17: 179-187. [17] Helenius T O, Misiorek J O, Nyström J H, et al.2015. Keratin 8 absence down-regulates colonocyte HMGCS2 and modulates colonic ketogenesis and energy metabolism[J]. Molecular Biology of the Cell, 26(12): 2298-2310. [18] Kang Y, Xie H, Zhao C.2019. Ankrd45 is a novel ankyrin repeat protein required for cell proliferation[J]. Genes (Basel), 10(6): 462. [19] Katata T, Irie K, Fukuhara A, et al.2003. Involvement of nectin in the localization of IQGAP1 at the cell-cell adhesion sites through the actin cytoskeleton in Madin-Darby canine kidney cells[J]. Oncogene, 22(14): 2097-109. [20] Kim D, Langmead B, Salzberg S L.2015. HISAT: A fast spliced aligner with low memory requirements[J]. Nature Methods, 12(4): 357-360. [21] Kumar D, Hassan M K, Pattnaik N, et al.2017. Reduced expression of IQGAP2 and higher expression of IQGAP3 correlates with poor prognosis in cancers[J]. PLOS ONE, 12(10): e0186977. [22] Lane M A, Jesse B W.1997. Effect of volatile fatty acid infusion on development of the rumen epithelium in neonatal sheep[J]. Journal of Dairy Science, 80(4): 740-746. [23] Liao Y, Smyth G K, Shi W.2014. feature Counts: An efficient general purpose program for assigning sequence reads to genomic features[J]. Bioinformatics, 30(7): 923-30. [24] Lin L, Xie F, Sun D, et al.2019. Ruminal microbiome-host crosstalk stimulates the development of the ruminal epithelium in a lamb model[J]. Microbiome, 7(1): 83. [25] Liu J, Bian G, Sun D, et al.2017. Starter feeding altered ruminal epithelial bacterial communities and some key immune-related genes' expression before weaning in lambs[J]. Journal of Animal Science, 95(2): 910-921. [26] Love M I, Huber W, Anders S.2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2[J]. Genome Biology, 15(12): 550. [27] Lv F, Wang X J, Pang X, et al.2020. Effects of supplementary feeding on the rumen morphology and bacterial diversity in lambs[J]. PeerJ, 8: e9353. [28] Malmuthuge N, Liang G, Guan LL.2019. Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes[J]. Genome Biology, 20(1): 172. [29] Miranda-Gonçalves V, Bezerra F, Costa-Almeida R, et al.2017. Monocarboxylate transporter 1 is a key player in glioma-endothelial cell crosstalk[J]. Molecular carcinogenesis, 56(12): 2630-2642. [30] Mizutani Y, Mitsutake S, Tsuji K, et al.2009. Ceramide biosynthesis in keratinocyte and its role in skin function[J]. Biochimie, 91(6): 784-790. [31] Moll R, Divo M, Langbein L.2008. The human keratins: Biology and pathology[J]. Histochemistry and Cell Biology, 129(6): 705-33. [32] Mortazavi A, Williams B A, Mccue K, et al.2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq[J]. Nature methods, 5(7): 621-628. [33] Mosavi L K, Cammett T J, Desrosiers DC, et al.2004. The ankyrin repeat as molecular architecture for protein recognition[J]. Protein Science. 13(6): 1435-1448. [34] Naeem A, Drackley J K, Lanier J S, et al.2014. Ruminal epithelium transcriptome dynamics in response to plane of nutrition and age in young Holstein calves[J]. Functional & integrative genomics, 14(1): 261-273. [35] Rizwan A N, Gerhard B.2007. Organicanion transporters of the SLC22 family: Biopharmaceutical, physiological, and pathological roles[J]. Pharmaceutical Research, 24(3): 450-470. [36] Robinson M D, Mccarthy D J, Smyth G K.2010. edgeR: A bioconductor package for differential expression analysis of digital gene expression data[J]. Bioinformatics, 26(1): 139-140. [37] Roh S G, Kuno M, Hishikawa D, et al.2007. Identification of differentially expressed transcripts in bovine rumen and abomasum using a differential display method[J]. Journal of Animal Science, 85(2): 395-403. [38] Roh S G, Suzuki Y, Gotoh T, et al.2016. Physiological roles of adipokines, hepatokines, and myokines in ruminants[J]. Asian-Australasian Journal of Animal Science, 29(1): 1-15. [39] Sakamoto K, Aragaki T, Morita K, et al.2011. Down-regulation of keratin 4 and keratin 13 expression in oral squamous cell carcinoma and epithelial dysplasia: A clue for histopathogenesis[J]. Histopathology, 58(4): 531-542. [40] Schmidt VA, Scudder L, Devoe CE, et al.2003. IQGAP2 functions as a GTP-dependent effector protein in thrombin-induced platelet cytoskeletal reorganization[J]. Blood, 101(8): 3021-3028. [41] Shen Z, Seyfert H M, Lohrke B, et al.2004. An energy-rich diet causes rumen papillae proliferation association with more IGF-1 type I receptors and increased plasma IGF-I concentrations in young goats[J].The Journal of Nutrition, 134(1): 11-7. [42] Sun D M, Mao S Y, Zhu W Y, et al.2018. Effect of starter diet supplementation on rumen epithelial morphology and expression of genes involved in cell proliferation and metabolism in pre-weaned lambs[J]. Animal, 12(11): 2274-2283. [43] Walter A, Hastings D, Gutknecht J.1982. Weak acid permeability through lipid bilayer membranes. Role of chemical reactions in the unstirred layer[J].The Journal of General Physiology, 79(5): 917-933. [44] Xiang R, McNally J, Rowe S, et al.2016. Gene network analysis identifiesrumen epithelial cell proliferation, differentiation and metabolicpathways perturbed by dietand correlated with methaneproduction[J]. Scientific Reports, 6: 39022. [45] Yamaoka-Tojo M, Ushio-Fukai M, Hilenski L, et al.2004. IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species- dependent endothelial migration and proliferation[J]. Circulation Research, 95(3): 276-283. [46] Zeisel SH.2012. Diet-gene interactions underlie metabolic individuality and influence brain development: Implications for clinical practice derived from studies on choline metabolism[J]. Annals of Nutrition & Metabolism, 60(Suppl 3): 19-25. |
|
|
|