Abstract
Animal body coverings provide protection and allow for adaptation to environmental pressures such as heat, ultraviolet radiation, water loss, and mechanical forces. Here, using a comparative genomics analysis of 39 mammal species spanning three skin covering types (hairless, scaly and spiny), we found some genes (e.g., UVRAG, POLH, and XPC) involved in skin inflammation, skin innate immunity, and ultraviolet radiation damage repair were under selection in hairless ocean mammals (e.g., whales and manatees). These signatures might be associated with a high risk of skin diseases from pathogens and ultraviolet radiation. Moreover, the genomes from three spiny mammal species shared convergent genomic regions (EPHB2, EPHA4, and NIN) and unique positively selected genes (FZD6, INVS, and CDC42) involved in skin cell polarity, which might be related to the development of spines. In scaly mammals, the shared convergent genomic regions (e.g., FREM2) were associated with the integrity of the skin epithelium and epidermal adhesion. This study identifies potential convergent genomic features among distantly related mammals with the same skin covering type.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Acevedo-Whitehouse, K., and Duffus, A.L.J. (2009). Effects of environmental change on wildlife health. Phil Trans R Soc B 364, 3429–3438.
Ajiro, M., Nishidate, T., Katagiri, T., and Nakamura, Y. (2010). Critical involvement of RQCD1 in the EGFR-Akt pathway in mammary carcinogenesis. Int J Oncol 37, 1085–1093.
Alibardi, L. (2003). Adaptation to the land: the skin of reptiles in comparison to that of amphibians and endotherm amniotes. J Exp Zool 298B, 12–41.
Baker, J. (1992). Skin disease in wild cetaceans from British waters. Aquat Mamm 18, 27–32.
Bandyopadhyay, A., Tsuji, K., Cox, K., Harfe, B.D., Rosen, V., and Tabin, C.J. (2006). Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2, e216.
Banerji, R., Eble, D.M., Iovine, M.K., and Skibbens, R.V. (2016). Esco2 regulates cx43 expression during skeletal regeneration in the zebrafish fin. Dev Dyn 245, 7–21.
Bao, W., Kojima, K.K., and Kohany, O. (2015). Repbase update, a database of repetitive elements in eukaryotic genomes. Mobile DNA 6, 11.
Barlow, J. (1984). Xenarthrans and pholidotes. In: Anderson, S., and Jones Jr, J.K., eds. Orders and Families of Recent Mammals of the World. New York: John Wiley & Sons. 219–239.
Bazzi, H., Fantauzzo, K.A., Richardson, G.D., Jahoda, C.A.B., and Christiano, A.M. (2007). Transcriptional profiling of developing mouse epidermis reveals novel patterns of coordinated gene expression. Dev Dyn 236, 961–970.
Benrebeh, I., Grati, M., Bonnet, C., Bouassida, W., Hadjamor, I., Ayadi, H., Ghorbel, A., Petit, C., and Masmoudi, S. (2016). Genetic analysis of Tunisian families with Usher syndrome type 1: toward improving early molecular diagnosis. Mol Vis 22, 827–835.
Benson, G. (1999). Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27, 513–580.
Bernstein, C., and Bernstein, H. (2015). Epigenetic reduction of DNA repair in progression to cancer. In: Chen, C., ed. Advances in DNA Repair. London: IntechOpen.
Bertulli, C., Cecchetti, A., van Bressem, M., and Van Waerebeek, K. (2012). Skin disorders in common minke whales and white-beaked dolphins off Iceland, a photographic assessment. J Marine Anim Ecol 5: 29–40.
Birney, E., Clamp, M., and Durbin, R. (2004). GeneWise and genomewise. Genome Res 14, 988–995.
Blume-Peytavi, U., Whiting, D.A., and Trüeb, R.M. (2008). Hair Growth and Disorders. Heidelberg: Springer.
Boratyn, G.M., Camacho, C., Cooper, P.S., Coulouris, G., Fong, A., Ma, N., Madden, T.L., Matten, W.T., McGinnis, S.D., Merezhuk, Y., et al. (2013). BLAST: a more efficient report with usability improvements. Nucleic Acids Res 41, W29–W33.
Botchkarev, V.A., and Fessing, M.Y. (2005). Edar signaling in the control of hair follicle development. J Invest Dermatol Sympos Proc 10, 247–251.
Burge, C., and Karlin, S. (1997). Prediction of complete gene structures in human genomic DNA. J Mol Biol 268, 78–94.
Bush, J.O., Lan, Y., and Jiang, R. (2004). The cleft lip and palate defects in Dancer mutant mice result from gain of function of the Tbx10 gene. Proc Natl Acad Sci USA 101, 7022–7027.
Cantarel, B.L., Korf, I., Robb, S.M.C., Parra, G., Ross, E., Moore, B., Holt, C., Sanchez Alvarado, A., and Yandell, M. (2008). MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18, 188–196.
Capecchi, M. (1997). Hox genes and mammalian development. Cold Spring Harb Symp Quant Biol, 62: 273–281.
Carpenter, E.M., Goddard, J.M., Davis, A.P., Nguyen, T.P., and Capecchi, M.R. (1997). Targeted disruption of Hoxd-10 affects mouse hindlimb development. Development 124, 4505–4514.
Chen, J., and Chuong, C.M. (2012). Patterning skin by planar cell polarity: the multi-talented hair designer. Exp Dermatol 21, 81–85.
Chereau, D., Kerff, F., Graceffa, P., Grabarek, Z., Langsetmo, K., and Dominguez, R. (2005). Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly. Proc Natl Acad Sci USA 102, 16644–16649.
Chernova, O.F., and Kuznetsov, G.V. (2001). Structural features of spines in some rodents (Rodentia: Myomorpha, Hystricomorpha). Biol Bull Rus Acad Sci 28, 371–383.
Choo, S.W., Rayko, M., Tan, T.K., Hari, R., Komissarov, A., Wee, W.Y., Yurchenko, A.A., Kliver, S., Tamazian, G., Antunes, A., et al. (2016). Pangolin genomes and the evolution of mammalian scales and immunity. Genome Res 26, 1312–1322.
Chrostek, A., Wu, X., Quondamatteo, F., Hu, R., Sanecka, A., Niemann, C., Langbein, L., Haase, I., and Brakebusch, C. (2006). Rac1 is crucial for hair follicle integrity but is not essential for maintenance of the epidermis. Mol Cell Biol 26, 6957–6970.
Chuong, C.M., and Homberger, D.G. (2003). Development and evolution of the amniote integument: current landscape and future horizon. J Exp Zool 298B, 1–11.
Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676.
Coutton, C., Vargas, A.S., Amiri-Yekta, A., Kherraf, Z.E., Ben Mustapha, S.F., Le Tanno, P., Wambergue-Legrand, C., Karaouzène, T., Martinez, G., Crouzy, S., et al. (2018). Mutations in CFAP43 and CFAP44 cause male infertility and flagellum defects in Trypanosoma and human. Nat Commun 9, 686.
Dai, D., Zhu, H., Wlodarczyk, B., Zhang, L., Li, L., Li, A.G., Finnell, R.H., Roop, D.R., and Chen, J. (2011). Fuz controls the morphogenesis and differentiation of hair follicles through the formation of primary cilia. J Invest Dermatol 131, 302–310.
De Bie, T., Cristianini, N., Demuth, J.P., and Hahn, M.W. (2006). CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269–1271.
Devasagayam, T., Tilak, J., Boloor, K., Sane, K.S., Ghaskadbi, S.S., and Lele, R. (2004). Free radicals and antioxidants in human health: current status and future prospects. J Assoc Physicans India 52, 794–804.
Devenport, D., and Fuchs, E. (2008). Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat Cell Biol 10, 1257–1268.
Di Lucca, J., Guedj, M., Lacapère, J.J., Fargnoli, M.C., Bourillon, A., Dieudé, P., Dupin, N., Wolkenstein, P., Aegerter, P., Saiag, P., et al. (2009). Variants of the xeroderma pigmentosum variant gene (POLH) are associated with melanoma risk. Eur J Cancer 45, 3228–3236.
Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797.
Etienne-Manneville, S., and Hall, A. (2003). Cdc42 regulates GSK-3β and adenomatous polyposis coli to control cell polarity. Nature 421, 753–756.
Feldhamer, G.A. (2007). Mammalogy: Adaptation, Diversity, Ecology. Maryland: Johns Hopkins University Press.
Foote, A.D., Liu, Y., Thomas, G.W.C., Vinař, T., Alföldi, J., Deng, J., Dugan, S., van Elk, C.E., Hunter, M.E., Joshi, V., et al. (2015). Convergent evolution of the genomes of marine mammals. Nat Genet 47, 272–275.
Franklin, C.C., Backos, D.S., Mohar, I., White, C.C., Forman, H.J., and Kavanagh, T.J. (2009). Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol Aspects Med 30, 86–98.
Gendron-Maguire, M., Mallo, M., Zhang, M., and Gridley, T. (1993). Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75, 1317–1331.
Geraci, J., St Aubin, D., and Hicks, B. (1986). The epidermis of odontocetes: a view from within. In: Bryden, M.M., and Harrison, R., eds. Research on Dolphins. Oxford: Oxford University Press. 3–21.
Guindon, S., Lethiec, F., Duroux, P., and Gascuel, O. (2005). PHYML Online—A web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33, W557–W559.
Gul, I.S., Hulpiau, P., Saeys, Y., and van Roy, F. (2017). Evolution and diversity of cadherins and catenins. Exp Cell Res 358, 3–9.
Guo, N., Hawkins, C., and Nathans, J. (2004). Frizzled6 controls hair patterning in mice. Proc Natl Acad Sci USA 101, 9277–9281.
Hahn, C., Bachmann, L., and Chevreux, B. (2013). Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res 41, e129.
Haq, S., Michael, A., Andreucci, M., Bhattacharya, K., Dotto, P., Walters, B., Woodgett, J., Kilter, H., and Force, T. (2003). Stabilization of β-catenin by a Wnt-independent mechanism regulates cardiomyocyte growth. Proc Natl Acad Sci USA 100, 4610–4615.
Hasegawa, M., Higashi, K., Yokoyama, C., Yamamoto, F., Tachibana, T., Matsushita, T., Hamaguchi, Y., Saito, K., Fujimoto, M., and Takehara, K. (2013). Altered expression of dermokine in skin disorders. J Eur Acad Dermatol Venereol 27, 867–875.
Hemnani, T., and Parihar, M. (1998). Reactive oxygen species and oxidative DNA damage. Indian J Physiol Pharm 42, 440–452.
Hoey, K.A., Wise, R.R., and Adler, G.H. (2004). Ultrastructure of echimyid and murid rodent spines. J Zool 263, 307–315.
Hogan, B.L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10, 1580–1594.
Holt, C., and Yandell, M. (2011). MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinf 12, 491.
Hong, Y.R., Chen, C.H., Chang, J.H., Wang, S., Sy, W.D., Chou, C.K., and Howng, S.L. (2000). Cloning and characterization of a novel human ninein protein that interacts with the glycogen synthase kinase 3β. Biochim Biophys Acta 1492, 513–516.
Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G., and Birchmeier, W. (2001). β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105, 533–545.
Hulpiau, P., and van Roy, F. (2009). Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 41, 349–369.
Jadeja, S., Smyth, I., Pitera, J.E., Taylor, M.S., van Haelst, M., Bentley, E., McGregor, L., Hopkins, J., Chalepakis, G., Philip, N., et al. (2005). Identification of a new gene mutated in Fraser syndrome and mouse myelencephalic blebs. Nat Genet 37, 520–525.
Jansson, L., Kim, G.S., and Cheng, A.G. (2015). Making sense of Wnt signaling—linking hair cell regeneration to development. Front Cell Neurosci 9.
Jung, Y.S., Liu, G., and Chen, X. (2010). Pirh2 E3 ubiquitin ligase targets DNA polymerase eta for 20S proteasomal degradation. Mol Cell Biol 30, 1041–1048.
Khan, I., Maldonado, E., Vasconcelos, V., O’Brien, S.J., Johnson, W.E., and Antunes, A. (2014). Mammalian keratin associated proteins (KRTAPs) subgenomes: disentangling hair diversity and adaptation to terrestrial and aquatic environments. BMC Genomics 15, 779.
Kim, E.B., Fang, X., Fushan, A.A., Huang, Z., Lobanov, A.V., Han, L., Marino, S.M., Sun, X., Turanov, A.A., Yang, P., et al. (2011). Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature 479, 223–227.
Kim, T.G., Kim, M., Lee, J.J., Kim, S.H., Je, J.H., Lee, Y., Song, M.J., Choi, Y., Chung, Y.W., Park, C.G., et al. (2015). CCCTC-binding factor controls the homeostatic maintenance and migration of Langerhans cells. J Allergy Clin Immunol 136, 713–724.
Kirkegaard, S.S., Wulff, T., Gammeltoft, S., and Hoffmann, E.K. (2013). KCNK5 is functionally down-regulated upon long-term hypotonicity in ehrlich ascites tumor cells. Cell Physiol Biochem 32, 1238–1246.
Lai-Cheong, J.E., and McGrath, J.A. (2009). Structure and function of skin, hair and nails. Medicine 37, 223–226.
Leistra, W., Hoyer, M., Kik, M., and Sinke, J. (2003). Recurrent skin problems in a manatee: the diagnostic approach. Tijdschr Diergeneeskd 128, 140–144.
Lewandoski, M., Sun, X., and Martin, G.R. (2000). Fgf8 signalling from the AER is essential for normal limb development. Nat Genet 26, 460–463.
Li, R., Zhu, H., Ruan, J., Qian, W., Fang, X., Shi, Z., Li, Y., Li, S., Shan, G., Kristiansen, K., et al. (2010). De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20, 265–272.
Lu, S.C. (2009). Regulation of glutathione synthesis. Mol Aspects Med 30, 42–59.
Majoros, W.H., Pertea, M., and Salzberg, S.L. (2004). TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879.
Marsh, H., O’Shea, T.J., and Reynolds III, J.E. (2011). Ecology and Conservation of the Sirenia: Dugongs and Manatees. Cambridge: Cambridge University Press.
Martinez-Levasseur, L.M., Gendron, D., Knell, R.J., O’Toole, E.A., Singh, M., and Acevedo-Whitehouse, K. (2011). Acute sun damage and photoprotective responses in whales. Proc R Soc B 278, 1581–1586.
Meyer, W., Liumsiricharoen, M., Suprasert, A., Fleischer, L.G., and Hewicker-Trautwein, M. (2013). Immunohistochemical demonstration of keratins in the epidermal layers of the Malayan pangolin (Manis javanica), with remarks on the evolution of the integumental scale armour. Eur J Histochem 57, 27.
Moll, R., Schiller, D.L., and Franke, W.W. (1990). Identification of protein IT of the intestinal cytoskeleton as a novel type I cytokeratin with unusual properties and expression patterns. J Cell Biol 111, 567–580.
Naso, M.F., Liang, B., Chris Huang, C., Song, X.Y., Shahied-Arruda, L., Belkowski, S.M., D’Andrea, M.R., Polkovitch, D.A., Lawrence, D.R., Griswold, D.E., et al. (2007). Dermokine: an extensively differentially spliced gene expressed in epithelial cells. J Invest Dermatol 127, 1622–1631.
Nelson, D.S., Halteren, A., Quispel, W.T., Bos, C., Bovée, J.V.M.G., Patel, B., Badalian-Very, G., Hummelen, P., Ducar, M., Lin, L., et al. (2015). MAP2K1 and MAP3K1 mutations in langerhans cell histiocytosis. Genes Chromosomes Cancer 54, 361–368.
Orange, J.S., Stone, K.D., Turvey, S.E., and Krzewski, K. (2004). The Wiskott-Aldrich syndrome. Cell Mol Life Sci 61, 2361–2385.
Panteleyev, A.A., Paus, R., Ahmad, W., Sundberg, J.P., and Christiano, A. M. (1998). Molecular and functional aspects of the hairless (hr) gene in laboratory rodents and humans. Exp Dermatol 7, 249–267.
Panteleyev, A.A., Botchkareva, N.V., Sundberg, J.P., Christiano, A.M., and Paus, R. (1999). The role of the hairless (hr) gene in the regulation of hair follicle catagen transformation. Am J Pathol 155, 159–171.
Po-Chedley, D.S., and Shadle, A.R. (1955). Pelage of the porcupine, Erethizon dorsatum dorsatum. J Mammal 36, 84–95.
Premi, S., Wallisch, S., Mano, C.M., Weiner, A.B., Bacchiocchi, A., Wakamatsu, K., Bechara, E.J.H., Halaban, R., Douki, T., and Brash, D. E. (2015). Chemiexcitation of melanin derivatives induces DNA photoproducts long after UV exposure. Science 347, 842–847.
Price, A.L., Jones, N.C., and Pevzner, P.A. (2005). De novo identification of repeat families in large genomes. Bioinformatics 21, i351–i358.
Prum, R.O., and Torres, R.H. (2004). Structural colouration of mammalian skin: convergent evolution of coherently scattering dermal collagen arrays. J Exp Biol 207, 2157–2172.
Pucci, S., Fisco, T., and Zonetti, M.J. (2012). XRCC5 (X-ray repair complementing defective repair in Chinese hamster cells 5 (double-strand-break rejoining)). Atlas Genets Cytogenets Oncol Haematol doi: https://doi.org/10.4267/2042/48234.
Ravni, A., Qu, Y., Goffinet, A.M., and Tissir, F. (2009). Planar cell polarity cadherin Celsr1 regulates skin hair patterning in the mouse. J Invest Dermatol 129, 2507–2509.
Ronquist, F., and Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
Rosas, F.C.W. (1994). Biology, conservation and status of the Amazonian manatee Trichechus inunguis. Mammal Rev 24, 49–59.
Samuelov, L., Sprecher, E., and Paus, R. (2015). The role of P-cadherin in skin biology and skin pathology: lessons from the hair follicle. Cell Tissue Res 360, 761–771.
Segade, F. (2010). Glucose transporter 10 and arterial tortuosity syndrome: the vitamin C connection. FEBS Lett 584, 2990–2994.
Sen, G.L., Reuter, J.A., Webster, D.E., Zhu, L., and Khavari, P.A. (2010). DNMT1 maintains progenitor function in self-renewing somatic tissue. Nature 463, 563–567.
Shapiro, M.D., Kronenberg, Z., Li, C., Domyan, E.T., Pan, H., Campbell, M., Tan, H., Huff, C.D., Hu, H., Vickrey, A.I., et al. (2013). Genomic diversity and evolution of the head crest in the rock pigeon. Science 339, 1063–1067.
Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V., and Zdobnov, E.M. (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212.
Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Krönig, C., Schermer, B., Benzing, T., Cabello, O.A., Jenny, A., et al. (2005). Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37, 537–543.
Smit, A.F., Hubley, R., and Green, P. (1996). RepeatMasker Open-3.0.
Song, H., Hu, J., Chen, W., Elliott, G., Andre, P., Gao, B., and Yang, Y. (2010). Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466, 378–382.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
Stanke, M., Keller, O., Gunduz, I., Hayes, A., Waack, S., and Morgenstern, B. (2006). AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res 34, W435–W439.
Stary, A., and Sarasin, A. (2001). XPC (xeroderma pigmentosum, complementation group C).
Stewart, G.S., Wang, B., Bignell, C.R., Taylor, A.M.R., and Elledge, S.J. (2003). MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961–966.
Suyama, M., Torrents, D., and Bork, P. (2006). PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34, W609–W612.
Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. System Biol 56, 564–577.
van Bressem, M.F., Reyes, J.C., Félix, F., Echegaray, M., Siciliano, S., Di Beneditto, A.P., Flach, L., Viddi, F., Avila, I.C., Herrera, J.C., et al. (2007). A preliminary overview of skin and skeletal diseases and traumata in small cetaceans from South American waters. Lat Am J Aquat Mamm 6, 7–42.
van Bressem, M.F., Raga, A.J., Di Guardo, G., Jepson, P.D., Duignan, P.J., Siebert, U., Barrett, T., Santos, M.O., Moreno, I.B., Siciliano, S., et al. (2009). Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis Aquat Org 86, 143–157.
Wang, Y., Chang, H., and Nathans, J. (2010). When whorls collide: the development of hair patterns in frizzled 6 mutant mice. Development 137, 4091–4099.
Wilson, B., Arnold, H., Bearzi, G., Fortuna, C.M., Gaspar, R., Ingram, S., Liret, C., Pribanic, S., Read, A.J., Ridoux, V., et al. (1999). Epidermal diseases in bottlenose dolphins: impacts of natural and anthropogenic factors. Proc R Soc Lond B 266, 1077–1083.
Wood, R.D., Mitchell, M., Sgouros, J., and Lindahl, T. (2001). Human DNA repair genes. Science 291, 1284–1289.
Wu, X., Quondamatteo, F., Lefever, T., Czuchra, A., Meyer, H., Chrostek, A., Paus, R., Langbein, L., and Brakebusch, C. (2006). Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. Genes Dev 20, 571–585.
Xu, Z., and Wang, H. (2007). LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35, W265–W268.
Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24, 1586–1591.
Yang, Y., He, S., Wang, Q., Li, F., Kwak, M.J., Chen, S., O’Connell, D., Zhang, T., Pirooz, S.D., Jeon, Y.H., et al. (2016). Autophagic UVRAG promotes UV-induced photolesion repair by activation of the CRL4 DDB2 E3 ligase. Mol Cell 62, 507–519.
Yim, H.S., Cho, Y.S., Guang, X., Kang, S.G., Jeong, J.Y., Cha, S.S., Oh, H. M., Lee, J.H., Yang, E.C., Kwon, K.K., et al. (2014). Minke whale genome and aquatic adaptation in cetaceans. Nat Genet 46, 88–92.
Yoshida, K., and Miki, Y. (2004). Role of BRCA1 and BRCA2 as regulators of DNA repair, transcription, and cell cycle in response to DNA damage. Cancer Sci 95, 866–871.
Yu, M., Finner, A., Shapiro, J., Lo, B., Barekatain, A., and McElwee, K.J. (2006). Hair follicles and their role in skin health. Expert Rev Dermatol 1, 855–871.
Zhou, J., Liu, M., Fleming, A.M., Burrows, C.J., and Wallace, S.S. (2013). Neil3 and NEIL1 DNA glycosylases remove oxidative damages from quadruplex DNA and exhibit preferences for lesions in the telomeric sequence context. J Biol Chem 288, 27263–27272.
Zhu, H., Enaw, J.O.E., Ma, C., Shaw, G.M., Lammer, E.J., and Finnell, R. H. (2007). Association between CFL1 gene polymorphisms and spina bifida risk in a California population. BMC Med Genet 8, 12.
Acknowledgements
This work was supported by the National Natural Science Fund for Outstanding Youth Fund (31222009, 31272295, 31570489, 81622048 and 81473377), the Project of Quality Guarantee System of Chinese Herbal Medicines (201507002), Science Foundation for Distinguished Young Scholars of Jiangsu Province (BK20140049) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Data availability
The raw genome datasets are deposited in NCBI (PRJNA490788 and PRJNA490787). The full gene list involved in this manuscript could be found in Table S32 in Supporting Information.
Compliance and ethics
The author(s) declare that they have no conflict of interest.
Supporting information
Rights and permissions
About this article
Cite this article
Cao, P., Dai, Q., Deng, C. et al. Genome-wide signatures of mammalian skin covering evolution. Sci. China Life Sci. 64, 1765–1780 (2021). https://doi.org/10.1007/s11427-020-1841-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-020-1841-5