Preliminary comparison of skin transcriptome from sheep with different wool fibre diameters
Yunxia Qi
A , Shaoyin Fu A C D , Xiaolong He A , Biao Wang A , Lai Da A , Rigele Te A , Ma Yuejun A , Sun Suzhen A , Wenguang Zhang B and Yongbin Liu A D
A Inner Mongolia Academy of Agricultural & Animal Husbandry Sciences, No. 22, Zhaojun Road, Yuquan District, Hohhot, Inner Mongolia, 010031 China.
B College of Animal Science, Inner Mongolia Agricultural University, No. 306, Zhaowuda Road, Saihan District, Hohhot, Inner Mongolia, 010018 China.
C Institute of ATCG, Nei Mongolia Bio-Information, No. 306, Zhaowuda Road, Saihan District, Hohhot, Inner Mongolia, 010018 China.
D Corresponding authors. Email: fushao1234@126.com; ybliu117@126.com
Animal Production Science 61(7) 708-714 https://doi.org/10.1071/AN19311
Submitted: 28 May 2019 Accepted: 9 December 2020 Published: 28 January 2021
Abstract
Context: Wool is one of the most important animal fibres for the textile industry, and its diameter directly affects its economic value. However, the molecular mechanisms underlying wool fibre diameter (FD) in sheep have not been fully elucidated.
Aims: The aims of the work were to make an initial comparison of skin transcriptomes from sheep with wool of high and low FD, and to identify key genes affecting FD.
Methods: High-throughput RNA-Seq technology was employed to explore the skin transcriptome, using three sheep with fine wool (FD <21.0 μm) and three sheep with coarse wool (FD >27.0 μm).
Key results: We obtained 28 607 228 bp of clean sequence data, 78.9% (±3.8%) of which uniquely aligned to the reference genome across the six samples. In total, 19 914 mRNA transcripts were expressed (FPKM >0) in the six skin samples, among which were certain well-known genes involved in the skin–hair cycle, such as KRTAP7-1, KRT14, Wnt10b, Wnt2b, β-catenin and FGF5. Furthermore, 467 genes were significantly differentially expressed between the fine-wool and coarse-wool groups, including 21 genes with upregulated and 446 genes with downregulated expression in the sheep with lower FD. These differentially expressed genes were particularly enriched in the gene ontology processes related to lipid metabolism, skin development, differentiation and immune function (P < 0.05). The biological processes were involved in collagen catabolism, negative regulation of macromolecule metabolism, steroid hormone stimulation and lipid metabolism. A significant Kyoto Encyclopedia of Genes and Genomes pathway involving the metabolism of lipids and lipoproteins was also enriched, revealing that lipid metabolism might be one of the key factors affecting FD. The expression of these differentially expressed genes that were involved in the metabolism of lipids and lipoproteins pathway was verified by quantitative real-time PCR (qPCR). The correlation between the mRNA expression level from qPCR and RNA-Seq data was 0.999 (P < 0.001).
Conclusions: The 467 differentially expressed genes, especially those involved in lipid metabolism and immune function, may play key roles in wool follicle metabolism and the expression of wool FD.
Implications: This study provided valuable data for future studies aimed at elucidating the mechanisms that underlie wool follicle metabolism and wool FD. The work may also have implications for studies of the human hair follicle.
Keywords: DEG, lipid metabolism, immune function, wool fibre diameter.
References
Amiria M, Yousefnia S, Forootan FS, Maryam P, Ghaedi K, Esfahanid MHN (2018) Diverse roles of fatty acid binding proteins (FABPs) in development and pathogenesis of cancers. Gene 676, 171–183.| Diverse roles of fatty acid binding proteins (FABPs) in development and pathogenesis of cancers.Crossref | GoogleScholarGoogle Scholar |
Cruz CF, Fernandes MM, Gomes AC, Coderch L, Martí M, Méndez S, Gales L, Azoia NG, Shimanovich U, Cavaco-Paulo A (2013) Keratins and lipids in ethnic hair. International Journal of Cosmetic Science 35, 244–249.
| Keratins and lipids in ethnic hair.Crossref | GoogleScholarGoogle Scholar | 23301816PubMed |
Dry FW (1955) The dominant N gene in New Zealand Romney sheep. Australian Journal of Agricultural Research 6, 725–769.
| The dominant N gene in New Zealand Romney sheep.Crossref | GoogleScholarGoogle Scholar |
Duvel L, Chun H, Deppa D, Wertz PW (2005) Analysis of hair lipids and tensile properties as a function of distance from scalp. International Journal of Cosmetic Science 27, 193–197.
| Analysis of hair lipids and tensile properties as a function of distance from scalp.Crossref | GoogleScholarGoogle Scholar | 18492187PubMed |
Fan R, Xie J, Bai J, Wang H, Tian X, Bai R, Jia X, Yang L, Song Y, Herrid M, Gao W, He X, Yao J, Smith GW, Dong C (2013) Skin transcriptome profiles associated with coat color in sheep. BMC Genomics 14, 389
| Skin transcriptome profiles associated with coat color in sheep.Crossref | GoogleScholarGoogle Scholar | 23758853PubMed |
Fonollosa J, Campos L, Martí M, de la Maza A, Parra JL, Coderch L (2004) X-ray diffraction analysis of internal wool lipids. Chemistry and Physics of Lipids 130, 159–166.
| X-ray diffraction analysis of internal wool lipids.Crossref | GoogleScholarGoogle Scholar | 15172832PubMed |
Fu SY, Qi YX, He XL, Da L, Wang B, Te RGL, Wu JH, Yang D, Liu YB, Zhang WG (2016) Transcriptome analysis reveals skin lipid metabolism related to wool diameter in sheep bioRxiv
| Transcriptome analysis reveals skin lipid metabolism related to wool diameter in sheepCrossref | GoogleScholarGoogle Scholar |
Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC, Spertus JA, Costa F (2006) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Current Opinion in Cardiology 21, 1–6.
| Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement.Crossref | GoogleScholarGoogle Scholar | 16355022PubMed |
Hepp D, Gonçalves GL, Moreira GR, de Freitas TR (2016) Epistatic interaction of the melanocortin 1 receptor and agouti signaling protein genes modulates wool color in the Brazilian Creole sheep. The Journal of Heredity 107, 544–552.
| Epistatic interaction of the melanocortin 1 receptor and agouti signaling protein genes modulates wool color in the Brazilian Creole sheep.Crossref | GoogleScholarGoogle Scholar | 27288530PubMed |
Hertzel AV, Bernlohr DA (2000) The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends in Endocrinology and Metabolism 11, 175–180.
| The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function.Crossref | GoogleScholarGoogle Scholar | 10856918PubMed |
McKillop IH, Girardi C, Thompson KJ (2019) Role of fatty acid binding proteins (FABPs) in cancer development and progression. Cellular Signalling 62, 109336
| Role of fatty acid binding proteins (FABPs) in cancer development and progression.Crossref | GoogleScholarGoogle Scholar | 31170472PubMed |
Jiang Y, Xie M, Chen W, Talbot R, Maddox JF, Faraut T, Wu C, Muzny DM, Li Y, Zhang W, Stanton JA, Brauning R, Barris WC, Hourlier T, Aken BL, Searle SMJ, Adelson DL, Bian C, Cam GR, Chen Y, Cheng S, DeSilva U, Dixen K, Dong Y, Fan G, Franklin IR, Fu S, Guan R, Highland MA, Holder ME, Huang G, Ingham AB, Jhangiani , Kalra D, Kovar CL, Lee SL, Liu W, Liu X, Lu C, Lv T, Mathew T, McWilliam S, Menzies M, Pan S, Robelin D, Servin B, Townley D, Wang W, Wei B, White SN, Yang X, Ye C, Yue Y, Zeng P, Zhou Q, Hansen JB, Kristensen K, Gibbs RA, Flicek P, Warkup CC, Jones HE, Oddy VH, Nicholas FW, McEwan JC, Kijas , Wang J, Worley KC, Archibald AL, Cockett N, Xu X, Wang W, Dalrymple BP (2014) The sheep genome illuminates biology of the rumen and lipid metabolism. Science 344, 1168–1173.
| The sheep genome illuminates biology of the rumen and lipid metabolism.Crossref | GoogleScholarGoogle Scholar | 24904168PubMed |
Jones LN, Rivett DE (1997) The role of 18-methyleicosanoic acid in the structure and formation of mammalian hair fibres. Micron 28, 469–485.
| The role of 18-methyleicosanoic acid in the structure and formation of mammalian hair fibres.Crossref | GoogleScholarGoogle Scholar | 9519472PubMed |
Kang X, Liu G, Liu Y, Xu Q, Zhang M, Fang M (2013) Transcriptome profile at different physiological stages reveals potential mode for curly fleece in Chinese Tan sheep. PLoS One 8, e71763
| Transcriptome profile at different physiological stages reveals potential mode for curly fleece in Chinese Tan sheep.Crossref | GoogleScholarGoogle Scholar | 24367566PubMed |
Kramer W, Girbig F, Gutjahr U, Kowalewski S, Jouvenal K, Müller G, Tripier D, Wess G (1993) Intestinal bile acid absorption. Na(+)-dependent bile acid transport activity in rabbit small intestine correlates with the coexpression of an integral 93-kDa and a peripheral 14-kDa bile acid-binding membrane protein along the duodenum-ileum axis. The Journal of Biological Chemistry 268, 18035–18046.
Lauvergne JJ, Dolling CHS, Renieri C, Broad TE, Maddox JF (1996) ‘Mendelian inheritance in sheep 1996 (Mis 96).’ (Comité de Nomenclature Genetique des Ovins et Caprins (COGOVICA): Clamart, France)
Liu H, Wang T, Wang J, Quan F, Zhang Y (2013a) Characterization of Liaoning cashmere goat transcriptome: sequencing, de novo assembly, functional annotation and comparative analysis. PLoS One 8, e77062
| Characterization of Liaoning cashmere goat transcriptome: sequencing, de novo assembly, functional annotation and comparative analysis.Crossref | GoogleScholarGoogle Scholar | 24391812PubMed |
Liu T, Zhu S, Tang Q, Chen P, Yu Y, Tang S (2013b) De novo assembly and characterization of transcriptome using Illumina, Inc. paired-end sequencing and identification of CesA gene in ramie (Boehmeria nivea L. Gaud). BMC Genomics 14, 125
| De novo assembly and characterization of transcriptome using Illumina, Inc. paired-end sequencing and identification of CesA gene in ramie (Boehmeria nivea L. Gaud).Crossref | GoogleScholarGoogle Scholar | 23442184PubMed |
Liu YX, Shi GQ, Wang HX, Wan PC, Tang H, Yang H, Guan F (2014) Polymorphisms of KAP6, KAP7, and KAP8 genes in four Chinese sheep breeds. Genetics and Molecular Research 13, 3438–3445.
| Polymorphisms of KAP6, KAP7, and KAP8 genes in four Chinese sheep breeds.Crossref | GoogleScholarGoogle Scholar | 24841789PubMed |
Maneli MH, Mkentane K, Khumalo NP (2013) Lipid distribution and influence on hair structure. International Journal of Cosmetic Science 35, 523
| Lipid distribution and influence on hair structure.Crossref | GoogleScholarGoogle Scholar | 23738587PubMed |
Masukawa Y, Narita H, Imokawa G (2005) Characterization of the lipid composition at the proximal root regions of human hair. Journal of Cosmetic Science 27, 191
| Characterization of the lipid composition at the proximal root regions of human hair.Crossref | GoogleScholarGoogle Scholar |
Matejuk A (2018) Skin immunity. Archivum Immunologiae et Therapiae Experimentalis 66, 45–54.
| Skin immunity.Crossref | GoogleScholarGoogle Scholar | 28623375PubMed |
Parsons YM, Cooper DW, Piper LR (1994) Evidence of linkage between high-glycine-tyrosine keratin gene loci and wool fibre diameter in a Merino half-sib family. Animal Genetics 25, 105–108.
| Evidence of linkage between high-glycine-tyrosine keratin gene loci and wool fibre diameter in a Merino half-sib family.Crossref | GoogleScholarGoogle Scholar | 7516629PubMed |
Ponz R, Moreno C, Allain D, Elsen JM, Lantier F, Lantier I, Brunel JC, Pérez-Enciso M (2001) Assessment of genetic variation explained by markers for wool traits in sheep via a segment mapping approach. Mammalian Genome 12, 569–572.
| Assessment of genetic variation explained by markers for wool traits in sheep via a segment mapping approach.Crossref | GoogleScholarGoogle Scholar | 11420622PubMed |
Purvis WI, Franklin IR (2005) Major genes and QTL influencing wool production and quality: a review. Genetics Selection Evolution 37, S97
| Major genes and QTL influencing wool production and quality: a review.Crossref | GoogleScholarGoogle Scholar |
Richmond JM, Harris JE (2014) Immunology and skin in health and disease. Cold Spring Harbor Perspectives in Medicine 4, a015339
| Immunology and skin in health and disease.Crossref | GoogleScholarGoogle Scholar | 25452424PubMed |
Schlossman ML, Mccarthy JP (1978) Lanolin and its derivatives. Journal of the American Oil Chemists’ Society 55, 447–450.
| Lanolin and its derivatives.Crossref | GoogleScholarGoogle Scholar |
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 3, 1101–1108.
| Analyzing real-time PCR data by the comparative C(T) method.Crossref | GoogleScholarGoogle Scholar | 18546601PubMed |
Storch J, Mcdermott L (2009) Structural and functional analysis of fatty acid-binding proteins. Journal of Lipid Research 50, S126–S131.
| Structural and functional analysis of fatty acid-binding proteins.Crossref | GoogleScholarGoogle Scholar | 19017610PubMed |
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7, 562–578.
| Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks.Crossref | GoogleScholarGoogle Scholar | 22383036PubMed |
Tuncman G, Erbay E, Hom X, Vivo IDe, Campos H, Rimm EB, Hotamisligil GS (2006) A genetic variant at the fatty acid-binding protein aP2 locus reduces the risk for hypertriglyceridemia, type 2 diabetes, and cardiovascular disease. Proceedings of the National Academy of Sciences of the United States of America 103, 6970–6975.
| A genetic variant at the fatty acid-binding protein aP2 locus reduces the risk for hypertriglyceridemia, type 2 diabetes, and cardiovascular disease.Crossref | GoogleScholarGoogle Scholar | 16641093PubMed |
Vicente R, Bolger AM, Martínez-Carrasco R, Pérez P, Gutiérrez E, Usadel B, Morcuende R (2019) De Novo transcriptome analysis of durum wheat flag leaves provides new insights into the regulatory response to elevated CO2 and high temperature. Frontiers in Plant Science 10, 1605
| De Novo transcriptome analysis of durum wheat flag leaves provides new insights into the regulatory response to elevated CO2 and high temperature.Crossref | GoogleScholarGoogle Scholar | 31921252PubMed |
Wertz PW, Downing DT (1988) Integral lipids of human hair. Lipids 23, 878–881.
| Integral lipids of human hair.Crossref | GoogleScholarGoogle Scholar | 3185123PubMed |
Yue Y, Guo T, Liu J, Guo J, Yuan C, Feng R, Niu C, Sun X, Yang B (2015a) Exploring differentially expressed genes and natural antisense transcripts in sheep (Ovis aries) skin with different wool fibre diameters by digital gene expression profiling. PLoS One 10, e0129249
| Exploring differentially expressed genes and natural antisense transcripts in sheep (Ovis aries) skin with different wool fibre diameters by digital gene expression profiling.Crossref | GoogleScholarGoogle Scholar | 26658757PubMed |
Yue YJ, Liu JB, Yang M, Han JL, Guo TT, Guo J, Feng RL, Yang BH (2015b) De novo assembly and characterization of skin transcriptome using RNAseq in sheep (Ovis aries). Genetics and Molecular Research 14, 1371–1384.
| De novo assembly and characterization of skin transcriptome using RNAseq in sheep (Ovis aries).Crossref | GoogleScholarGoogle Scholar | 25730076PubMed |
