Volume 43 Issue 4
Jul.  2022
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Yuan Yuan, Da-Ming Sun, Tao Qin, Sheng-Yong Mao, Wei-Yun Zhu, Yu-Yang Yin, Jie Huang, Rasmus Heller, Zhi-Peng Li, Jun-Hua Liu, Qiang Qiu. Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies. Zoological Research, 2022, 43(4): 634-647. doi: 10.24272/j.issn.2095-8137.2022.086
Citation: Yuan Yuan, Da-Ming Sun, Tao Qin, Sheng-Yong Mao, Wei-Yun Zhu, Yu-Yang Yin, Jie Huang, Rasmus Heller, Zhi-Peng Li, Jun-Hua Liu, Qiang Qiu. Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies. Zoological Research, 2022, 43(4): 634-647. doi: 10.24272/j.issn.2095-8137.2022.086

Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies

doi: 10.24272/j.issn.2095-8137.2022.086
#Authors contributed equally to this work
Funds:  This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA26040301-02), National Natural Science Foundation of China (31970392, 32172752, 32122083), Research Funds for Interdisciplinary Subject of NWPU (19SH030408), Funds Awarded by the 1000 Talent Project of Shaanxi Province, Project for Top Young Talents Program of College of Animal Science and Technology of Nanjing Agricultural University (DKQB201904), and Talents Team Construction Fund of Jilin Agricultural University.
More Information
  • As an important evolutionary innovation and unique organ, the rumen has played a crucial role in ruminant adaptation to complex ecological environments. However, the cellular basis of its complex morphology and function remains largely unknown. In this study, we identified eight major cell types from seven representative prenatal and postnatal rumen samples using ~56 600 single-cell transcriptomes. We captured the dynamic changes and high heterogeneity in cellular and molecular profiles before, during, and after the appearance of keratinized stratified squamous epithelium with neatly arranged papillae and functional maturity. Basal cells, keratinocytes, differentiating keratinocytes, terminally differentiated keratinocytes, and special spinous cells provided the cellular basis for rumen epithelium formation. Notably, we obtained clear evidence of two keratinization processes involved in early papillogenesis and papillae keratinization and identified TBX3 as a potential marker gene. Importantly, enriched stratum spinosum cells played crucial roles in volatile fatty acid (VFA) metabolism and immune response. Our results provide a comprehensive transcriptional landscape of rumen development at single-cell resolution, as well as valuable insight into the interactions between dietary metabolism and the rumen.
  • #Authors contributed equally to this work
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  • [1]
    Baldwin RL, Connor EE. 2017. Rumen function and development. Veterinary Clinics of North America:Food Animal Practice, 33(3): 427−439. doi: 10.1016/j.cvfa.2017.06.001
    [2]
    Beharka AA, Nagaraja TG, Morrill JL, Kennedy GA, Klemm RD. 1998. Effects of form of the diet on anatomical, microbial, and fermentative development of the rumen of neonatal calves. Journal of Dairy Science, 81(7): 1946−1955. doi: 10.3168/jds.S0022-0302(98)75768-6
    [3]
    Bond JJ, Donaldson AJ, Coumans JVF, Austin K, Ebert D, Wheeler D, et al. 2019. Protein profiles of enzymatically isolated rumen epithelium in sheep fed a fibrous diet. Journal of Animal Science and Biotechnology, 10(1): 5. doi: 10.1186/s40104-019-0314-0
    [4]
    Bragulla HH, Homberger DG. 2009. Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. Journal of Anatomy, 214(4): 516−559. doi: 10.1111/j.1469-7580.2009.01066.x
    [5]
    Brychtova V, Coates PJ, Hrabal V, Boldrup L, Fabian P, Vojtesek B, et al. 2020. Keratin 36, a specific marker of tongue filiform papillae, is downregulated in squamous cell carcinoma of the mobile tongue. Molecular and Clinical Oncology, 12(5): 421−428.
    [6]
    Candi E, Schmidt R, Melino G. 2005. The cornified envelope: a model of cell death in the skin. Nature reviews Molecular Cell Biology, 6(4): 328–340.
    [7]
    Chen L, Qiu Q, Jiang Y, Wang K, Lin ZS, Li ZP, et al. 2019. Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits. Science, 364(6446): eaav6202. doi: 10.1126/science.aav6202
    [8]
    Cochain C, Vafadarnejad E, Arampatzi P, Pelisek J, Winkels H, Ley K, et al. 2018. Single-cell RNA-seq reveals the transcriptional landscape and heterogeneity of aortic macrophages in murine atherosclerosis. Circulation Research, 122(12): 1661−1674. doi: 10.1161/CIRCRESAHA.117.312509
    [9]
    Finnegan A, Cho RJ, Luu A, Harirchian P, Lee J, Cheng JB, et al. 2019. Single-cell transcriptomics reveals spatial and temporal turnover of keratinocyte differentiation regulators. Frontiers in Genetics, 10: 775. doi: 10.3389/fgene.2019.00775
    [10]
    Fonty G, Jouany JP, Chavarot M, Bonnemoy F, Gouet P. 1991. Development of the rumen digestive functions in lambs placed in a sterile isolator a few days after birth. Reproduction Nutrition Development, 31(5): 521−528. doi: 10.1051/rnd:19910504
    [11]
    Franco A, Masot J, Redondo E. 2011. Ontogenesis of the rumen: a comparative analysis of the Merino sheep and Iberian red deer. Animal Science Journal, 82(1): 107−116. doi: 10.1111/j.1740-0929.2010.00814.x
    [12]
    Frank DU, Carter KL, Thomas KR, Burr RM, Bakker ML, Coetzee WA, et al. 2012. Lethal arrhythmias in Tbx3-deficient mice reveal extreme dosage sensitivity of cardiac conduction system function and homeostasis. Proceedings of the National Academy of Sciences of the United States of America, 109(3): E154−E163.
    [13]
    Gao N, Me R, Dai C, Yu FSX. 2020. ISG15 acts as a mediator of innate immune response to Pseudomonas aeruginosa infection in C57BL/6J mouse corneas. Investigative Ophthalmology & Visual Science, 61(5): 26−26.
    [14]
    Gao S, Sun Y, Zhang XB, Hu LM, Liu YX, Chua CY, et al. 2016. IGFBP2 activates the NF-κB pathway to drive epithelial–mesenchymal transition and invasive character in pancreatic ductal adenocarcinoma. Cancer Research, 76(22): 6543−6554. doi: 10.1158/0008-5472.CAN-16-0438
    [15]
    García A, Masot J, Franco A, Gázquez A, Redondo E. 2012. Histomorphometric and immunohistochemical study of the goat rumen during prenatal development. The Anatomical Record:Advances in Integrative Anatomy and Evolutionary Biology, 295(5): 776−785. doi: 10.1002/ar.22431
    [16]
    Giesecke D, Beck U, Wiesmayr S, Stangassinger M. 1979. The effect of rumen epithelial development on metabolic activities and ketogenesis by the tissue in vitro. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 62(4): 459–463.
    [17]
    Graham C, Simmons NL. 2005. Functional organization of the bovine rumen epithelium. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 288(1): R173−R181. doi: 10.1152/ajpregu.00425.2004
    [18]
    Groenewald HB. 1993. Ultrastructure of the epithelium of the rumen, reticulum and omasum of grey, white and black karakul lambs. Onderstepoort Journal of Veterinary Research, 60(3): 197−204.
    [19]
    Guo JT, Sosa E, Chitiashvili T, Nie XC, Rojas EJ, Oliver E, et al. 2021. Single-cell analysis of the developing human testis reveals somatic niche cell specification and fetal germline stem cell establishment. Cell Stem Cell, 28(4): 764−778.e4. doi: 10.1016/j.stem.2020.12.004
    [20]
    Haber AL, Biton M, Rogel N, Herbst RH, Shekhar K, Smillie C, et al. 2017. A single-cell survey of the small intestinal epithelium. Nature, 551(7680): 333−339. doi: 10.1038/nature24489
    [21]
    Han XP, Zhou ZM, Fei LJ, Sun HY, Wang RY, Chen Y, et al. 2020. Construction of a human cell landscape at single-cell level. Nature, 581(7808): 303−309. doi: 10.1038/s41586-020-2157-4
    [22]
    Jenkins G, Tortora GJ. 2016. Anatomy and Physiology. 6th ed. Hoboken: John Wiley & Sons.
    [23]
    Joost S, Zeisel A, Jacob T, Sun XY, La Manno G, Lönnerberg P, et al. 2016. Single-cell transcriptomics reveals that differentiation and spatial signatures shape epidermal and hair follicle heterogeneity. Cell Systems, 3(3): 221−237.e9. doi: 10.1016/j.cels.2016.08.010
    [24]
    Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M. 2021. KEGG: integrating viruses and cellular organisms. Nucleic Acids Research, 49(D1): D545−D551. doi: 10.1093/nar/gkaa970
    [25]
    Khan SF, Damerell V, Omar R, Du Toit M, Khan M, Maranyane HM, et al. 2020. The roles and regulation of TBX3 in development and disease. Gene, 726: 144223. doi: 10.1016/j.gene.2019.144223
    [26]
    Kim SH, Turnbull J, Guimond S. 2011. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. Journal of Endocrinology, 209(2): 139−151. doi: 10.1530/JOE-10-0377
    [27]
    Lei Y, Zhang K, Guo MM, Li GW, Li C, Li BB, et al. 2018. Exploring the spatial-temporal microbiota of compound stomachs in a pre-weaned goat model. Frontiers in Microbiology, 9: 1846. doi: 10.3389/fmicb.2018.01846
    [28]
    Ma ASP, Ozers LJ. 1996. Annexins I and II show differences in subcellular localization and differentiation-related changes in human epidermal keratinocytes. Archives of Dermatological Research, 288(10): 596−603. doi: 10.1007/BF02505262
    [29]
    Martini F. 2006. Anatomy and Physiology'2007 Ed. Rex Bookstore, Inc.
    [30]
    Masunaga T, Shimizu H, Ishiko A, Fujiwara T, Hashimoto T, Nishikawa T. 1995. Desmoyokin/AHNAK protein localizes to the non-desmosomal keratinocyte cell surface of human epidermis. Journal of Investigative Dermatology, 104(6): 941−945. doi: 10.1111/1523-1747.ep12606213
    [31]
    Mehic D, Bakiri L, Ghannadan M, Wagner EF, Tschachler E. 2005. Fos and jun proteins are specifically expressed during differentiation of human keratinocytes. Journal of Investigative Dermatology, 124(1): 212−220. doi: 10.1111/j.0022-202X.2004.23558.x
    [32]
    Mizrahi I, Jami E. 2018. Review: The compositional variation of the rumen microbiome and its effect on host performance and methane emission. Animal, 12(s2): s220−s232.
    [33]
    Naeem A, Drackley JK, Stamey J, Loor JJ. 2012. Role of metabolic and cellular proliferation genes in ruminal development in response to enhanced plane of nutrition in neonatal Holstein calves. Journal of Dairy Science, 95(4): 1807−1820. doi: 10.3168/jds.2011-4709
    [34]
    Ogawa E, Owada Y, Ikawa S, Adachi Y, Egawa T, Nemoto K, et al. 2011. Epidermal FABP (FABP5) regulates keratinocyte differentiation by 13(S)-HODE-mediated activation of the NF-κB signaling pathway. Journal of Investigative Dermatology, 131(3): 604−612. doi: 10.1038/jid.2010.342
    [35]
    Oshima T, Gedda K, Koseki J, Chen X, Husmark J, Watari J, et al. 2011. Establishment of esophageal-like non-keratinized stratified epithelium using normal human bronchial epithelial cells. American Journal of Physiology-Cell Physiology, 300(6): C1422−C1429. doi: 10.1152/ajpcell.00376.2010
    [36]
    Pan XY, Wang Y, Li ZJ, Chen XQ, Heller R, Wang NN, et al. 2020. Tracing the origin of a new organ by inferring the genetic basis of rumen evolution. bioRxiv,doi: 10.1101/2020.02.19.955872.
    [37]
    Pazoki A, Ghorbani GR, Kargar S, Sadeghi-Sefidmazgi A, Drackley JK, Ghaffari MH. 2017. Growth performance, nutrient digestibility, ruminal fermentation, and rumen development of calves during transition from liquid to solid feed: Effects of physical form of starter feed and forage provision. Animal Feed Science and Technology, 234: 173−185. doi: 10.1016/j.anifeedsci.2017.06.004
    [38]
    Peres J, Mowla S, Prince S. 2015. The T-box transcription factor, TBX3, is a key substrate of AKT3 in melanomagenesis. Oncotarget, 6(3): 1821−1833. doi: 10.18632/oncotarget.2782
    [39]
    Perng YC, Lenschow DJ. 2018. ISG15 in antiviral immunity and beyond. Nature Reviews Microbiology, 16(7): 423−439. doi: 10.1038/s41579-018-0020-5
    [40]
    Prenzler F, Fragasso A, Schmitt A, Munz B. 2016. Functional analysis of ZFP36 proteins in keratinocytes. European Journal of Cell Biology, 95(8): 277−284. doi: 10.1016/j.ejcb.2016.04.007
    [41]
    Rémond D, Ortigues I, Jouany JP. 1995. Energy substrates for the rumen epithelium. Proceedings of the Nutrition Society, 54(1): 95−105. doi: 10.1079/PNS19950040
    [42]
    Russell JB, Rychlik JL. 2001. Factors that alter rumen microbial ecology. Science, 292(5519): 1119−1122. doi: 10.1126/science.1058830
    [43]
    Schoenberger SP. 2012. CD69 guides CD4+ T cells to the seat of memory. Proceedings of the National Academy of Sciences of the United States of America, 109(22): 8358−8359. doi: 10.1073/pnas.1204616109
    [44]
    Steele MA, AlZahal O, Hook SE, Croom J, Mcbride BW. 2009. Ruminal acidosis and the rapid onset of ruminal parakeratosis in a mature dairy cow: a case report. Acta Veterinaria Scandinavica, 51(1): 39. doi: 10.1186/1751-0147-51-39
    [45]
    Steven AC, Steinert PM. 1994. Protein composition of cornified cell envelopes of epidermal keratinocytes. Journal of Cell Science, 107(2): 693−700. doi: 10.1242/jcs.107.2.693
    [46]
    Steven D, Marshall A, Phillipson A. 1970. Organization of the rumen epithelium. Physiology of digestion and metabolism in the ruminant. In: Proceedings of the third international symposium. Cambridge, England, Newcastle-upon-Tyne: Oriel Press.
    [47]
    Storesund T, Schenck K, Osmundsen H, Røed A, Helgeland K, Kolltveit KM. 2009. Signal transduction and gene transcription induced by TFF3 in oral keratinocytes. European Journal of Oral Sciences, 117(5): 511−517. doi: 10.1111/j.1600-0722.2009.00652.x
    [48]
    Underwood WJ, Blauwiekel R, Delano ML, Gillesby R, Mischler SA, Schoell A. 2015. Biology and diseases of ruminants (sheep, goats, and cattle). In: Fox JG, Anderson LC, Otto GM, Pritchett-Corning KR, Whary MT. Laboratory Animal Medicine. Amsterdam: Elsevier, 623–694.
    [49]
    Vijayan A, Guha D, Ameer F, Kaziri I, Mooney CC, Bennett L, et al. 2013. IGFBP-5 enhances epithelial cell adhesion and protects epithelial cells from TGFβ1-induced mesenchymal invasion. The International Journal of Biochemistry & Cell Biology, 45(12): 2774−2785.
    [50]
    Wagner T, Beer L, Gschwandtner M, Eckhart L, Kalinina P, Laggner M, et al. 2019. The differentiation-associated keratinocyte protein cornifelin contributes to cell-cell adhesion of epidermal and mucosal keratinocytes. Journal of Investigative Dermatology, 139(11): 2292−2301.9. doi: 10.1016/j.jid.2019.04.019
    [51]
    Wang SX, Drummond ML, Guerrero-Juarez CF, Tarapore E, MacLean AL, Stabell AR, et al. 2020. Single cell transcriptomics of human epidermis identifies basal stem cell transition states. Nature Communications, 11(1): 4239. doi: 10.1038/s41467-020-18075-7
    [52]
    Wang YO, Brieher WM. 2020. CD2AP links actin to PI3 kinase activity to extend epithelial cell height and constrain cell area. Journal of Cell Biology, 219(1): e201812087. doi: 10.1083/jcb.201812087
    [53]
    Wani SA, Sahu AR, Khan RIN, Pandey A, Saxena S, Hosamani N, et al. 2019. Contrasting gene expression profiles of monocytes and lymphocytes from peste-des-petits-ruminants virus infected goats. Frontiers in Immunology, 10: 1463. doi: 10.3389/fimmu.2019.01463
    [54]
    Webster JD, Vucic D. 2020. The balance of TNF mediated pathways regulates inflammatory cell death signaling in healthy and diseased tissues. Frontiers in Cell and Developmental Biology, 8: 365. doi: 10.3389/fcell.2020.00365
    [55]
    Wise GH, Anderson GW. 1939. Factors affecting the passage of liquids into the rumen of the dairy calf. I. Method of administering liquids: drinking from open pail versus sucking through a rubber nipple. Journal of Dairy Science, 22(9): 697−705. doi: 10.3168/jds.S0022-0302(39)92926-7
    [56]
    Xia C, Braunstein Z, Toomey AC, Zhong JX, Rao XQ. 2018. S100 proteins As an important regulator of macrophage inflammation. Frontiers in Immunology, 8: 1908. doi: 10.3389/fimmu.2017.01908
    [57]
    Xu QB, Qiao QQ, Gao Y, Hou JX, Hu MY, Du YF, et al. 2021. Gut microbiota and their role in health and metabolic disease of dairy cow. Frontiers in Nutrition, 8: 701511. doi: 10.3389/fnut.2021.701511
    [58]
    Yang Z, Bowles NE, Scherer SE, Taylor MD, Kearney DL, Ge SP, et al. 2006. Desmosomal dysfunction due to mutations in desmoplakin causes arrhythmogenic right ventricular dysplasia/cardiomyopathy. Circulation Research, 99(6): 646−655. doi: 10.1161/01.RES.0000241482.19382.c6
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