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Transcriptome analysis of sika deer in China

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Abstract

Sika deer is of great commercial value because their antlers are used in tonics and alternative medicine and their meat is healthy and delicious. The goal of this study was to generate transcript sequences from sika deer for functional genomic analyses and to identify the transcripts that demonstrate tissue-specific, age-dependent differential expression patterns. These sequences could enhance our understanding of the molecular mechanisms underlying sika deer growth and development. In the present study, we performed de novo transcriptome assembly and profiling analysis across ten tissue types and four developmental stages (juvenile, adolescent, adult, and aged) of sika deer, using Illumina paired-end tag (PET) sequencing technology. A total of 1,752,253 contigs with an average length of 799 bp were generated, from which 1,348,618 unigenes with an average length of 590 bp were defined. Approximately 33.2 % of these (447,931 unigenes) were then annotated in public protein databases. Many sika deer tissue-specific, age-dependent unigenes were identified. The testes have the largest number of tissue-enriched unigenes, and some of them were prone to develop new functions for other tissues. Additionally, our transcriptome revealed that the juvenile-adolescent transition was the most complex and important stage of the sika deer life cycle. The present work represents the first multiple tissue transcriptome analysis of sika deer across four developmental stages. The generated data not only provide a functional genomics resource for future biological research on sika deer but also guide the selection and manipulation of genes controlling growth and development.

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References

  • Abba S, Galetto L, Carle P, Carrere S, Delledonne M, Foissac X, Palmano S, Veratti F, Marzachi C (2014) RNA-Seq profile of flavescence doree phytoplasma in grapevine. BMC Genom 15:1088

    Article  Google Scholar 

  • Borsy A, Podani J, Steger V, Balla B, Horvath A, Kosa JP, Gyurjan I Jr, Molnar A, Szabolcsi Z, Szabo L, Jako E, Zomborszky Z, Nagy J, Semsey S, Vellai T, Lakatos P, Orosz L (2009) Identifying novel genes involved in both deer physiological and human pathological osteoporosis. Mol Genet Genomics 281:301–313

    Article  CAS  PubMed  Google Scholar 

  • Garber M, Grabherr MG, Guttman M, Trapnell C (2011) Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods 8:469–477

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Seco D, Zhang Y, Gutierrez-Manero FJ, Martin C, Ramos-Solano B (2015) RNA-Seq analysis and transcriptome assembly for blackberry (Rubus sp. Var. Lochness) fruit. BMC Genom 16:5

    Article  CAS  Google Scholar 

  • Ghaffari N, Sanchez-Flores A, Doan R, Garcia-Orozco KD, Chen PL, Ochoa-Leyva A, Lopez-Zavala AA, Carrasco JS, Hong C, Brieba LG, Rudino-Pinera E, Blood PD, Sawyer JE, Johnson CD, Dindot SV, Sotelo-Mundo RR, Criscitiello MF (2014) Novel transcriptome assembly and improved annotation of the whiteleg shrimp (Litopenaeus vannamei), a dominant crustacean in global seafood mariculture. Sci Rep 4:7081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gyurjan I Jr, Molnar A, Borsy A, Steger V, Hackler L Jr, Zomborszky Z, Papp P, Duda E, Deak F, Lakatos P, Puskas LG, Orosz L (2007) Gene expression dynamics in deer antler: mesenchymal differentiation toward chondrogenesis. Mol Genet Genomics 277:221–235

    Article  CAS  PubMed  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Hao L, Li P, Yan L (2011) Analysis of expressed sequence tags (ESTs) in sika deer (Cervus nippon hortulorum) velvet tip tissue. Hereditas 33:371–377

    Article  CAS  PubMed  Google Scholar 

  • Hishiki T, Kawamoto S, Morishita S, Okubo K (2000) BodyMap: a human and mouse gene expression database. Nucleic Acids Res 28:136–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hobbs M, Pavasovic A, King AG, Prentis PJ, Eldridge MD, Chen Z, Colgan DJ, Polkinghorne A, Wilkins MR, Flanagan C, Gillett A, Hanger J, Johnson RN, Timms P (2014) A transcriptome resource for the koala (Phascolarctos cinereus): insights into koala retrovirus transcription and sequence diversity. BMC Genom 15:786

    Article  Google Scholar 

  • Kaiser VB, Bachtrog D (2014) De novo transcriptome assembly reveals sex-specific selection acting on evolving neo-sex chromosomes in Drosophila miranda. BMC Genom 15:241

    Article  Google Scholar 

  • Khudyakov JI, Preeyanon L, Champagne CD, Ortiz RM, Crocker DE (2015) Transcriptome analysis of northern elephant seal (Mirounga angustirostris) muscle tissue provides a novel molecular resource and physiological insights. BMC Genom 16:64

    Article  CAS  Google Scholar 

  • Kotsyfakis M, Schwarz A, Erhart J, Ribeiro JM (2015) Tissue- and time-dependent transcription in Ixodes ricinus salivary glands and midguts when blood feeding on the vertebrate host. Sci Rep 5:9103

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang HY, Carlson JE, Leebens-Mack JH, Wall PK, Mueller LA, Buzgo M, Landherr LL, Hu Y, DiLoreto DS, Ilut DC, Field D, Tanksley SD, Ma H, dePamphilis CW (2008) An EST database for Liriodendron tulipifera L. floral buds: the first EST resource for functional and comparative genomics in Liriodendron. Tree Genet Genomes 4:419–433

    Article  Google Scholar 

  • Lin GH, Wang K, Deng XG, Nevo E, Zhao F, Su JP, Guo SC, Zhang TZ, Zhao H (2014) Transcriptome sequencing and phylogenomic resolution within Spalacidae (Rodentia). BMC Genom 15:32

    Article  Google Scholar 

  • Liu H, Wang T, Wang J, Quan F, Zhang Y (2013) Characterization of Liaoning cashmere goat transcriptome: sequencing, de novo assembly, functional annotation and comparative analysis. PLoS One 8:e77062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittapalli O, Bai X, Mamidala P, Rajarapu SP, Bonello P, Herms DA (2010) Tissue-specific transcriptomics of the exotic invasive insect pest emerald ash borer (Agrilus planipennis). PLoS One 5:e13708

    Article  PubMed  PubMed Central  Google Scholar 

  • Molnar A, Gyurjan I, Korpos E, Borsy A, Steger V, Buzas Z, Kiss I, Zomborszky Z, Papp P, Deak F, Orosz L (2007) Identification of differentially expressed genes in the developing antler of red deer Cervus elaphus. Mol Genet Genomics 277:237–248

    Article  CAS  PubMed  Google Scholar 

  • Shen L, Liu G, Zou Y, Zhou Z, Su Z, Gu X (2015) The evolutionary panorama of organ-specifically expressed or repressed orthologous genes in nine vertebrate species. PLoS One 10:e0116872

    Article  PubMed  PubMed Central  Google Scholar 

  • Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145

    Article  CAS  PubMed  Google Scholar 

  • Soumillon M, Necsulea A, Weier M, Brawand D, Zhang X, Gu H, Barthes P, Kokkinaki M, Nef S, Gnirke A, Dym M, de Massy B, Mikkelsen TS, Kaessmann H (2013) Cellular source and mechanisms of high transcriptome complexity in the mammalian testis. Cell Rep 3:2179–2190

    Article  CAS  PubMed  Google Scholar 

  • Steger V, Molnar A, Borsy A, Gyurjan I, Szabolcsi Z, Dancs G, Molnar J, Papp P, Nagy J, Puskas L, Barta E, Zomborszky Z, Horn P, Podani J, Semsey S, Lakatos P, Orosz L (2010) Antler development and coupled osteoporosis in the skeleton of red deer Cervus elaphus: expression dynamics for regulatory and effector genes. Mol Genet Genomics 284:273–287

    Article  CAS  PubMed  Google Scholar 

  • Szuwart T, Kierdorf H, Kierdorf U, Clemen G (2002) Histochemical and ultrastructural studies of cartilage resorption and acid phosphatase activity during antler growth in fallow deer (Dama dama). Anat Rec 268:66–72

    Article  CAS  PubMed  Google Scholar 

  • Tian C, Tek Tay W, Feng H, Wang Y, Hu Y, Li G (2015) Characterization of Adelphocoris suturalis (Hemiptera: Miridae) transcriptome from different developmental stages. Sci Rep 5:11042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JP, Lindsay BG, Leebens-Mack J, Cui L, Wall K, Miller WC, dePamphilis CW (2004) EST clustering error evaluation and correction. Bioinformatics 20:2973–2984

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao B, Zhao Y, Wang Q, Zhang M, Liu M, Liu H, Li J (2012a) De novo characterization of the antler tip of Chinese Sika deer transcriptome and analysis of gene expression related to rapid growth. Mol Cell Biochem 364:93–100

    Article  CAS  PubMed  Google Scholar 

  • Yao B, Zhao Y, Zhang H, Zhang M, Liu M, Liu H, Li J (2012b) Sequencing and de novo analysis of the Chinese Sika deer antler-tip transcriptome during the ossification stage using Illumina RNA-Seq technology. Biotechnol Lett 34:813–822

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Fuscoe JC, Zhao C, Guo C, Jia M, Qing T, Bannon DI, Lancashire L, Bao W, Du T, Luo H, Su Z, Jones WD, Moland CL, Branham WS, Qian F, Ning B, Li Y, Hong H, Guo L, Mei N, Shi T, Wang KY, Wolfinger RD, Nikolsky Y, Walker SJ, Duerksen-Hughes P, Mason CE, Tong W, Thierry-Mieg J, Thierry-Mieg D, Shi L, Wang C (2014) A rat RNA-Seq transcriptomic BodyMap across 11 organs and 4 developmental stages. Nat Commun 5:3230

    PubMed  PubMed Central  Google Scholar 

  • Yue YJ, Liu JB, Yang M, Han JL, Guo TT, Guo J, Feng RL, Yang BH (2015) De novo assembly and characterization of skin transcriptome using RNAseq in sheep (Ovis aries). Genet Mol Res 14:1371–1384

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Yao B, Zhang M, Wang S, Zhang H, Xiao W (2013) Comparative analysis of differentially expressed genes in Sika deer antler at different stages. Mol Biol Rep 40:1665–1676

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank staff from the Institute of Special Economic Animals and Plants and State Key Laboratory for Molecular Biology of Special Economical Animals, Chinese Academy of Agricultural Sciences, for help in sika deer tissue collection. Illumina sequencing was performed at the Novogene Bioinformatics Technology Co., Ltd., Beijing, China. This study was Funded by grants from the Engineering of Scientific Innovation of the Chinese Academy of Agricultural Sciences.

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    Authors and Affiliations

    1. State Key Laboratory for Molecular Biology of Special Economical Animals, Institute of Special Economic Animals and Plants, Chinese Academy of Agricultural Sciences, 4899 Juye Street, Changchun, 130112, China

      Bo-Yin Jia, Heng-Xing Ba, Gui-Wu Wang, Ying Yang, Xue-Zhe Cui, Ying-Hua Peng, Jun-Jun Zheng, Xiu-Mei Xing & Fu-He Yang

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    1. Bo-Yin Jia
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    Correspondence to Fu-He Yang.

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    The authors declare that they have no conflicts of interest.

    Ethical approval

    The deer were euthanized and slaughtered in strict accordance with the local slaughtering procedure approved by the Animal Ethics Committee of the Institute of Special Wild Economic Animals and Plants, Chinese Academy of Agricultural Sciences.

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    Communicated by S. Hohmann.

    B.-Y. Jia and H.-X. Ba contributed to this manuscript equally.

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    Jia, BY., Ba, HX., Wang, GW. et al. Transcriptome analysis of sika deer in China. Mol Genet Genomics 291, 1941–1953 (2016). https://doi.org/10.1007/s00438-016-1231-y

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