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RNA-Seq-based transcriptome analysis of reproduction- and growth-related genes in Lateolabrax japonicus ovaries at four different ages

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Abstract

Lateolabrax japonicus is an abundant marine aquatic fish species that is commonly cultured in East Asia due to its high commercial value. In this study, RNA-Seq analysis of L. japonicus was carried out to identify reproduction- and growth-related genes expressed in L. japonicus ovaries at different ages using Illumina sequencing technology. In total, 334,388,688 high-quality reads were obtained in four libraries, i.e., 4-year-old ovaries (4th_Ovary), 3-year-old ovaries (3rd_Ovary), 2-year-old ovaries (2nd_Ovary), and 1-year-old ovaries (1st_Ovary). The reads were then de novo assembled into 101,860 unigenes with an average unigene length of 879 bp. In total, 30,142 unigenes (29.59%) were annotated in public databases, including Nr database (Nr), Swiss-Prot, Kyoto Encyclopedia of Genes and Genomes (KEGG), and Cluster of Orthologous Groups of proteins (COG), based on sequence similarity. Comparative analysis revealed that there were 35,749, 43,657, and 36,819 differentially expressed genes (DEGs) in three comparisons (4th_Ovary versus 3rd_Ovary, 4th_Ovary versus 2rd_Ovary, and 4th_Ovary versus 1st_Ovary, respectively). In total, 24,295 DEGs were different expressed in 4th_Ovary. Enrichment and pathway analyses of the DEGs were also carried out to excavate the candidate genes related to reproduction and growth, and 402 genes that potential involved in the regulation of reproduction and growth were identified, e.g., GnRHR (GnRH receptor), GHR 2 (growth hormone receptor 2), I_LGF1R (insulin-like growth factor 1 receptor), etc. Our findings expanded the genomic resources of L. japonicus and provided fundamental information for further studies.

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References

  1. Schuler G, Boguski M, Stewart E, Stein L, Gyapay G, Rice K, White R, Rodriguez-Tome P, Aggarwal A, Bajorek E (1996) A gene map of the human genome. Science 274(5287):540–546

    Article  CAS  Google Scholar 

  2. Dietrich WF, Miller J, Steen R, Merchant MA, Damron-Boles D, Husain Z, Dredge R, Daly MJ, Ingalls KA, O’Connor TJ (1996) A comprehensive genetic map of the mouse genome. Nature 380(6570):149–152

    Article  CAS  Google Scholar 

  3. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L (2010) The genome of the Western clawed frog Xenopus tropicalis. Science 328(5978):633–636

    Article  CAS  Google Scholar 

  4. Groenen MA, Cheng HH, Bumstead N, Benkel BF, Briles WE, Burke T, Burt DW, Crittenden LB, Dodgson J, Hillel J (2000) A consensus linkage map of the chicken genome. Genome Res 10(1):137–147

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Postlethwait JH, Yan Y-L, Gates MA, Horne S, Amores A, Brownlie A, Donovan A, Egan ES, Force A, Gong Z (1998) Vertebrate genome evolution and the zebrafish gene map. Nat Genet 18(4):345–349

    Article  CAS  Google Scholar 

  6. Wang W, Wu X, Liu Z, Zheng H, Cheng Y (2014) Insights into hepatopancreatic functions for nutrition metabolism and ovarian development in the crab Portunus trituberculatus: gene discovery in the comparative transcriptome of different hepatopancreas stages. PLoS ONE 9(1):e84921

    Article  Google Scholar 

  7. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5(4):288–298

    Article  CAS  Google Scholar 

  8. Venkatesh B (2003) Evolution and diversity of fish genomes. Curr Opin Genet Dev 13(6):588–592

    Article  CAS  Google Scholar 

  9. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447(7145):714–719

    Article  CAS  Google Scholar 

  10. Xiang L-x, He D, Dong W-r, Zhang Y-w, Shao J-z (2010) Deep sequencing-based transcriptome profiling analysis of bacteria-challenged Lateolabrax japonicus reveals insight into the immune-relevant genes in marine fish. BMC Genomics 11(1):472

    Article  Google Scholar 

  11. Hegedűs Z, Zakrzewska A, Ágoston VC, Ordas A, Rácz P, Mink M, Spaink HP, Meijer AH (2009) Deep sequencing of the zebrafish transcriptome response to mycobacterium infection. Mol Immunol 46(15):2918–2930

    Article  Google Scholar 

  12. Stockhammer OW, Zakrzewska A, Hegedûs Z, Spaink HP, Meijer AH (2009) Transcriptome profiling and functional analyses of the zebrafish embryonic innate immune response to Salmonella infection. J Immunol 182(9):5641–5653

    Article  CAS  Google Scholar 

  13. Xie Z, Xiao l, Wang D, Fang C, Liu Q, Li Z, Liu X, Zhang Y, Li S, Lin H (2014) Transcriptome analysis of the Trachinotus ovatus: identification of reproduction, growth and immune-related genes and microsatellite markers. PLos ONE 9(10):e109419

    Article  Google Scholar 

  14. Garg R, Patel RK, Tyagi AK, Jain M (2011) De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res 18(1):53–63

    Article  CAS  Google Scholar 

  15. Gjerde B (1986) Growth and reproduction in fish and shellfish. Aquaculture 57(1):37–55

    Article  Google Scholar 

  16. Sarà G, Reid G, Rinaldi A, Palmeri V, Troell M, Kooijman S (2012) Growth and reproductive simulation of candidate shellfish species at fish cages in the Southern Mediterranean: Dynamic Energy Budget (DEB) modelling for integrated multi-trophic aquaculture. Aquaculture 324:259–266

    Article  Google Scholar 

  17. Le Gac F, Blaise O, Fostier A, Le Bail P-Y, Loir M, Mourot B, Weil C (1993) Growth hormone (GH) and reproduction: a review. Fish Physiol Biochem 11(1–6):219–232

    Article  Google Scholar 

  18. Donelson J, Munday P, McCormick M, Pitcher C (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2(1):30–32

    Article  Google Scholar 

  19. Runnalls TJ, Beresford N, Losty E, Scott AP, Sumpter JP (2013) Several synthetic progestins with different potencies adversely affect reproduction of fish. Environ Sci Technol 47(4):2077–2084

    Article  CAS  Google Scholar 

  20. Schreck CB, Contreras-Sanchez W, Fitzpatrick MS (2001) Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 197(1):3–24

    Article  Google Scholar 

  21. Zhenzhen X, Ling X, Dengdong W, Chao F, Qiongyu L, Zihao L, Xiaochun L, Yong Z, Shuisheng L, Haoran L (2014) Transcriptome analysis of the Trachinotus ovatus: identification of reproduction, growth and immune-related genes and microsatellite markers. PLoS ONE 9(10):e109419

    Article  Google Scholar 

  22. Wang W, Yi Q, Ma L, Zhou X, Zhao H, Wang X, Qi J, Yu H, Wang Z, Zhang Q (2014) Sequencing and characterization of the transcriptome of half-smooth tongue sole (Cynoglossus semilaevis). BMC Genomics 15(1):470

    Article  CAS  Google Scholar 

  23. Reading BJ, Chapman RW, Schaff JE, Scholl EH, Opperman CH, Sullivan CV (2012) An ovary transcriptome for all maturational stages of the striped bass (Morone saxatilis), a highly advanced perciform fish. BMC Res Notes 5(1):111

    Article  CAS  Google Scholar 

  24. Men K, Ai Q, Mai K, Xu W, Zhang Y, Zhou H (2014) Effects of dietary corn gluten meal on growth, digestion and protein metabolism in relation to IGF-I gene expression of Japanese seabass, Lateolabrax japonicus. Aquaculture 428:303–309

    Article  Google Scholar 

  25. Wang J, Ai Q, Mai K, Xu H, Zuo R, Xu W, Zhang W, Zhang C (2014) Effects of dietary ethoxyquin on growth, feed utilization and residue in the muscle of juvenile Japanese seabass, Lateolabrax japonicus. Aquac Res 46(11):2656–2664

    Article  Google Scholar 

  26. Li Y, Ai Q, Mai K, Xu W, Deng J, Cheng Z (2014) Comparison of high-protein soybean meal and commercial soybean meal partly replacing fish meal on the activities of digestive enzymes and aminotransferases in juvenile Japanese seabass, Lateolabrax japonicus (Cuvier, 1828). Aquac Res 45(6):1051–1060

    Article  CAS  Google Scholar 

  27. Jia P, Jia K-T, Yi M-S (2015) Complete genome sequence of a fish nervous necrosis virus isolated from sea perch (Lateolabrax japonicus) in China. Genome Announc 3(3):e00048–e00015

    Article  Google Scholar 

  28. Xue M, Luo L, Wu X, Ren Z, Gao P, Yu Y, Pearl G (2006) Effects of six alternative lipid sources on growth and tissue fatty acid composition in Japanese sea bass (Lateolabrax japonicus). Aquaculture 260(1):206–214

    Article  CAS  Google Scholar 

  29. Wang Y, Cong B, Shen J, Liu S, Liu F, Wang N, Huang X (2012) Molecular cloning and functional analysis of a voltage-gated potassium channel in lymphocytes from sea perch, Lateolabrax japonicus. Fish Shellfish Immunol 33(3):605–613

    Article  CAS  Google Scholar 

  30. C. Zhang, M. Li (2005) Advance of study on reproductive biology and breeding technology of Lateolabrax aponicus. J Ningbo Univ (Nat Sci Eng Edn) 3:032

    Google Scholar 

  31. Kang DY, Han HK, Baek HJ (2002) Monthly gonadal and sex hormonal changes of indoor-reared seabass, Lateolabrax japonicus during annual reproductive cycle. Korean J Fish Aquat Sci 35(6):614–620

    CAS  Google Scholar 

  32. Hayashi I (1972) On the ovarian maturation of the Japanese sea bass, Lateolabrax japonicus. Jpn J Ichthyol 19(4):243–254

    Google Scholar 

  33. Xu J, Yan B, Teng Y, Lou G, Lu Z (2010) Analysis of nutrient composition and fatty acid profiles of Japanese sea bass Lateolabrax japonicus (Cuvier) reared in seawater and freshwater. J Food Compos Anal 23(5):401–405

    Article  CAS  Google Scholar 

  34. Xu B, Zhang P, Miao H, Li D, Moriyama S, Kawauchi H (1997) Isolation and bioactivity of growth hormone from Japanese seabass Lateolabrax japonicus. Acta Zool Sin 44(2):170–178

    CAS  Google Scholar 

  35. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JG, Korf I, Lapp H (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12(10):1611–1618

    Article  CAS  Google Scholar 

  36. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652

    Article  CAS  Google Scholar 

  37. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    Article  CAS  Google Scholar 

  38. Boeckmann B, Bairoch A, Apweiler R, Blatter M-C, Estreicher A, Gasteiger E, Martin MJ, Michoud K, O’Donovan C, Phan I (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 31(1):365–370

    Article  CAS  Google Scholar 

  39. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform 4(1):41

    Article  Google Scholar 

  40. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30

    Article  CAS  Google Scholar 

  41. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    Article  CAS  Google Scholar 

  42. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(suppl 2):W293–W297

    Article  CAS  Google Scholar 

  43. Audic S, Claverie J-M (1997) The significance of digital gene expression profiles. Genome Res 7(10):986–995

    Article  CAS  Google Scholar 

  44. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95(25):14863–14868

    Article  CAS  Google Scholar 

  45. Saldanha AJ (2004) Java Treeview—extensible visualization of microarray data. Bioinformatics 20(17):3246–3248

    Article  CAS  Google Scholar 

  46. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  47. Long Y, Li Q, Zhou B, Song G, Li T, Cui Z (2013) De novo assembly of mud loach (Misgurnus anguillicaudatus) skin transcriptome to identify putative genes involved in immunity and epidermal mucus secretion. PLoS ONE 8(2):e56998

    Article  CAS  Google Scholar 

  48. Wu J, Stoica BA, Dinizo M, Pajoohesh-Ganji A, Piao C, Faden AI (2012) Delayed cell cycle pathway modulation facilitates recovery after spinal cord injury. Cell Cycle 11(9):1782–1795

    Article  CAS  Google Scholar 

  49. Du Y-X, Ma K-Y, Qiu G-F (2015) Discovery of the genes in putative GnRH signaling pathway with focus on characterization of GnRH-like receptor transcripts in the brain and ovary of the oriental river prawn Macrobrachium nipponense. Aquaculture 442:1–11

    Article  CAS  Google Scholar 

  50. Shi Y, He M (2014) Differential gene expression identified by RNA-Seq and qPCR in two sizes of pearl oyster (Pinctada fucata). Gene 538(2):313–322

    Article  CAS  Google Scholar 

  51. Ge G, Xiao P, Zhang Y, Yang L (2011) The first insight into the tissue specific taxus transcriptome via Illumina second generation sequencing. PLoS ONE 6(6):e21220

    Article  Google Scholar 

  52. Salem M, Rexroad CE, Wang J, Thorgaard GH, Yao J (2010) Characterization of the rainbow trout transcriptome using Sanger and 454-pyrosequencing approaches. BMC Genomics 11(1):564

    Article  Google Scholar 

  53. Mair GC, Abucay JS, Beardmore JA, Skibinski DO (1995) Growth performance trials of genetically male tilapia (GMT) derived from YY-males in Oreochromis niloticus L.: on station comparisons with mixed sex and sex reversed male populations. Aquaculture 137(1):313–323

    Article  Google Scholar 

  54. Palmieri JR (1977) Host-induced morphological variations in the strigeoid trematode posthodiplostomum minimum (trematoda: diplostomatidae). ii. body measurements and tegument modifications. Gt Basin Nat 37(2):129–137

    Google Scholar 

  55. Guraya SS, Kaur R, Saxena PK (1975) Morphology of ovarian changes during the reproductive cycle of the fish Mystus tengara (Ham.). Cells Tissues Organs 91(2):222–260

    Article  CAS  Google Scholar 

  56. Schmid AC, Näf E, Kloas W, Reinecke M (1999) Insulin-like growth factor-I and-II in the ovary of a bony fish, Oreochromis mossambicus, the tilapia: in situ hybridisation, immunohistochemical localisation, Northern blot and cDNA sequences. Mol Cell Endocrinol 156(1):141–149

    Article  CAS  Google Scholar 

  57. Lo HW, Xia W, Wei Y, Ali-Seyed M, Huang SF, Hung MC (2005) Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Can Res 65(1):338–348

    CAS  Google Scholar 

  58. Zhou P, Liu DJ, Cang M, Ma YZ, Yang DS, Li HJ, Wang LM, Bou S, Feng HL (2008) TGFα and EGFR in ovine preimplantation embryos and effects on development. Anim Reprod Sci 104(2–4):370–381

    Article  CAS  Google Scholar 

  59. Gothilf Y, Elizur A, Chow M, Chen TT, Zohar Y (1995) Molecular cloning and characterization of a novel gonadotropin-releasing hormone from the gilthead seabream (Sparus aurata). Mol Mar Biol Biotechnol 4(1):27

    CAS  PubMed  Google Scholar 

  60. Jansen HT, Cutter C, Hardy S, Lehman MN, Goodman RL (2003) Seasonal plasticity within the gonadotropin-releasing hormone (GnRH) system of the ewe: changes in identified GnRH inputs and glial association. Endocrinology 144(8):3663–3676

    Article  CAS  Google Scholar 

  61. Kuiper GG, Enmark E, Peltohuikko M, Nilsson S, Gustafsson JA (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93(12):5925

    Article  CAS  Google Scholar 

  62. Leung YK, Mak P, Hassan S, Ho SM (2006) Estrogen receptor (ER)-β isoforms: a key to understanding ER-β signaling. Proc Natl Acad Sci USA 103(35):13162–13167

    Article  CAS  Google Scholar 

  63. Kitano T, Koyanagi T, Adachi R, Sakimura N, Takamune K, Abe SI (2006) Assessment of estrogenic chemicals using an estrogen receptor α (ERα)- and ERβ-mediated reporter gene assay in fish. Mar Biol 149(1):49–55

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by The Central Public-Interest Scientific Institution Basal Research Fund, South China Sea Fisheries Research Institute, CAFS (2017YB03, 2017YB28 and 2018ZD01); the Natural Science Foundation of China (3180228), the Natural Science Foundation of Guangdong Province, China (c18140500000602).

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Authors and Affiliations

  1. South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, China

    Chao Zhao, Pengfei Wang & Lihua Qiu

  2. Key Laboratory of South China Sea Fishery Resources Exploitation & Utilization, Ministry of Agriculture, Guangzhou, China

    Chao Zhao & Pengfei Wang

  3. Key Laboratory of Aquatic Genomics, Ministry of Agriculture, CAFS, Beijing, 100141, China

    Lihua Qiu

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  1. Chao Zhao
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Contributions

LHQ initiated the project. CZ performed bioinformatics analyses, designed experiments, carried out experiments, analyzed the data and interpreted results and wrote the manuscript. PFW reviewed the manuscript.

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Correspondence to Lihua Qiu.

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Additional File 1. Unigenes annotated by BLASTX against Nr, Swiss-Prot, COG, and KEGG. (XLSX 13819 KB)

11033_2018_4383_MOESM2_ESM.xlsx

Additional File 2. The functional classification of the COG classes for the transcriptome of Lateolabrax japonicus. (XLSX 122 KB)

11033_2018_4383_MOESM3_ESM.xlsx

Additional File 3. The functional classification of the GO classes for the transcriptome of Lateolabrax japonicus. (XLSX 309 KB)

Additional File 4. KEGG pathway analysis for the transcriptome of Lateolabrax japonicus. (XLSX 18 KB)

11033_2018_4383_MOESM5_ESM.xlsx

Additional File 5. Differentially expressed genes in 4th_Ovary versus 3rd_Ovary, 4th_Ovary versus 2rd_Ovary, and 4th_Ovary versus 1st_Ovary (FDR ≤ 0.001 AND |log2 ratio| ≥ 1). (XLSX 14929 KB)

Additional File 6. Differentially expressed genes enriched in 4th_Ovary. (XLSX 4032 KB)

Additional File 7. Novel candidate genes related to reproduction and growth were screened. (XLSX 132 KB)

Additional File 8. Primer sequences for semi-quantitative RT-PCR and quantitative RT-PCR. (XLSX 13 KB)

Supplementary material 9 (XLSX 10 KB)

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Zhao, C., Wang, P. & Qiu, L. RNA-Seq-based transcriptome analysis of reproduction- and growth-related genes in Lateolabrax japonicus ovaries at four different ages. Mol Biol Rep 45, 2213–2225 (2018). https://doi.org/10.1007/s11033-018-4383-5

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