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Fish Physiology and Biochemistry

, Volume 44, Issue 2, pp 435–449 | Cite as

Bioinformatic analyses of zona pellucida genes in vertebrates and their expression in Nile tilapia

  • Tianli Wu
  • Yunying Cheng
  • Zhilong Liu
  • Wenjing Tao
  • Shuqing Zheng
  • Deshou Wang
Article
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Abstract

Zona pellucida (ZP) genes encode ZP glycoproteins which constitute the coat surrounding oocytes and early embryos. Genome-wide identification of ZP genes is still lacking in vertebrates, especially in fish species. Herein, we conducted bioinformatic analyses of the ZP genes of the Nile tilapia and other vertebrates. Totally 16, 9, 17, 27, 21, 20, 26, 19, 14,11, 24, 17, 9, 18, 8, 11, 9, 8, 5, and 4 ZP genes belonging to 5 subfamilies (ZPA, ZPB, ZPC, ZPD, and ZPAX) were found in the sea lamprey, elephant shark, coelacanth, spotted gar, zebrafish, medaka, stickleback, Nile tilapia, Amazon molly, platyfish, seahorse, Northern snakehead, cavefish, tetraodon, clawed frog, turtle, chicken, platypus, kangaroo rat, and human genomes, respectively. The expansion of ZP genes in basal vertebrates was mainly achieved by gene duplication of ZPB, ZPC, and ZPAX subfamilies, while the shrink of ZP gene number in viviparous mammals was achieved by keeping only one copy of the ZP genes in each subfamily or even secondary loss of some subfamilies. The number of ZP gene is related to the environment where the eggs are fertilized and the embryos develop in vertebrates. Transcriptomic analysis showed that 14 ZP genes were expressed in the ovary of Nile tilapia, while two (ZPB2b and ZPC2) were highly expressed in the liver. On the other hand, ZPB1a and ZPB2c were not found to be expressed in any tissue or at any developmental stage of the gonads examined. In the ovary, the expression of ZP genes started from 30 dah (days after hatching), significantly upregulated at 90 dah and maintained this level at 180 dah. The expression of ZPC2 in the liver and ZPC5-2 and ZPAX1 in the ovary was confirmed by in situ hybridization. The ovary- and liver-expressed ZP genes are expressed coordinately with oocyte growth in tilapia.

Keywords

Zona pellucida genes Isolation Expression profile Nile tilapia Adaptive evolution 

Abbreviations

ZP

zona pellucida

ZPG

zona pellucida glycoprotein

VE

vitelline envelope

CTP

C-terminal propeptide

CFCS

consensus furin cleavage site

TMD

transmembrane domain

dah

days after hatching

FPKM

reads per kb per million reads

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Notes

Author contributions

Tianli Wu contributed to the preparation of the manuscript and analysis of the ZP genes. Yunying Cheng and Wenjing Tao carried out the sequence identification, contributed to the phylogenetic and transcriptomic analysis, and manually annotated the ZP genes. Zhilong Liu and Shuqing Zheng conducted experimental validation of expression data. Deshou Wang coordinated the study and was responsible for the final drafting of the manuscript. All authors read and approved the manuscript.

Funding information

This work was supported by grants 31630082, 91331119, and 31502147 from the National Natural Science Foundation of China and grant cstc2015jcyjB80001 from the Natural Science Foundation Project of Chongqing, Chongqing Science and Technology Commission.

Compliance with ethical standards

All animal experiments were undertaken in accordance with the National Institute of Health Guide for the Care and Use of Laboratory Animals, with the approval of the Scientific Investigation Board of Southwest University, Chongqing.

Competing interests

The authors declare that they have no competing interests.

Supplementary material

10695_2017_434_MOESM1_ESM.doc (947 kb)
ESM 1 (DOC 947 kb).

References

  1. Barisone GA, Krapf D, Correa-Fiz F, Arranz SE, Cabada MO (2007) Glycoproteins of the vitelline envelope of Amphibian oocyte: biological and molecular characterization of ZPC component (gp41) in Bufo arenarum. Mol Reprod Dev 74:629–640CrossRefPubMedGoogle Scholar
  2. Bausek N, Waclawek M, Schneider WJ, Wohlrab F (2000) The major chicken egg envelope protein ZP1 is different from ZPB and is synthesized in the liver. J Biol Chem 275:28866–28872CrossRefPubMedGoogle Scholar
  3. Beebe SJ, Leyton L, Burks D, Ishikawa M, Fuerst T, Dean J, Saling P (1992) Recombinant mouse ZP3 inhibits sperm binding and induces the acrosome reaction. Dev Biol 151:48–54CrossRefPubMedGoogle Scholar
  4. Berg AH, Westerlund L, Olsson PE (2004) Regulation of Arctic char (Salvelinus alpinus) egg shell proteins and vitellogenin during reproduction and in response to 17beta–estradiol and cortisol. Gen Comp Endocrinol 135:276–285CrossRefPubMedGoogle Scholar
  5. Bleil JD, Wassarman PM (1980a) Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev Biol 76:185–202CrossRefPubMedGoogle Scholar
  6. Bleil JD, Wassarman PM (1980b) Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20:873–882CrossRefPubMedGoogle Scholar
  7. Bleil JD, Wassarman PM (1983) Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev Biol 95:317–324CrossRefPubMedGoogle Scholar
  8. Bleil JD, Greve JM, Wassarman PM (1988) Identification of a secondary sperm receptor in the mouse egg zona pellucida: role in maintenance of binding of crosome-reacted sperm to eggs. Dev Biol 128:376–385CrossRefPubMedGoogle Scholar
  9. Boja ES, Hoodbhoy T, Fales HM, Dean J (2003) Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J Biol Chem 278:34189–34202CrossRefPubMedGoogle Scholar
  10. Cao L, Huang Q, Wu Z, Cao DD, Ma Z, Xu Q, Hu P, Fu Y, Shen Y, Chan J, Zhou CZ, Zhai W, Chen L (2016) Neofunctionalization of zona pellucida proteins enhances freeze-prevention in the eggs of Antarctic notothenioids. Nat Commun 7:12987CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chang YS, Wang SC, Tsao CC, Huang FL (1996) Molecular cloning, structural analysis, and expression of carp ZP3 gene. Mol Reprod Dev 44:295–304CrossRefPubMedGoogle Scholar
  12. Chang YS, Hsu CC, Wang SC, Tsao CC, Huang FL (1997) Molecular cloning, structural analysis, and expression of carp ZP2 gene. Mol Reprod Dev 46:258–267CrossRefPubMedGoogle Scholar
  13. Cheng YY, Tao WJ, Chen JL, Sun LN, Zhou LY, Song Q, Wang DS (2015) Genome-wide identification, evolution and expression analysis of nuclear receptor superfamily in Nile tilapia, Oreochromis niloticus. Gene 569:141–152CrossRefPubMedGoogle Scholar
  14. Claw KG, Swanson WJ (2012) Evolution of the egg: new findings and challenges. Annu Rev Genomics Hum Genet 13:109–125CrossRefPubMedGoogle Scholar
  15. Conner SJ, Hughes DC (2003) Analysis of fish ZP1/ZPB homologous genes-evidence for both genome duplication and species-specific amplification models of evolution. Reproduction 126:347–352CrossRefPubMedGoogle Scholar
  16. Conner SJ, Lefièvre L, Hughes DC, Barratt CL (2005) Cracking the egg: increased complexity in the zona pellucida. Hum Reprod 5:1148–1152CrossRefGoogle Scholar
  17. Del Giacco L, Diani S, Cotelli F (2000) Identification and spatial distribution of the mRNA encoding an egg envelope component of the Cyprinid zebrafish, Danio rerio, homologous to the mammalian ZP3 (ZPC). Dev Genes Evol 210(1):41–46CrossRefPubMedGoogle Scholar
  18. Fan LC, Yang ST, Gui JF (2001) Differential screening and characterization analysis of the egg envelope glycoprotein ZP3 cDNAs between gynogenetic and gonochoristic crucian carp. Cell Res 1:17–27CrossRefGoogle Scholar
  19. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefPubMedGoogle Scholar
  20. Feng R, Fang L, Cheng Y, He X, Jiang W, Dong R, Shi H, Jiang D, Sun L, Wang D (2015) Retinoic acid homeostasis through aldh1a2 and cyp26a1 mediates meiotic entry in Nile tilapia (Oreochromis niloticus). Sci Rep 5:10131CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fujita T, Fukada H, Shimizu M, Hiramatsu N, Hara A (2008) Molecular cloning and characterization of three distinct choriogenins in masu salmon, Oncorhynchus masou. Mol Reprod 75:1217–1228CrossRefGoogle Scholar
  22. Ganguly A, Bansal P, Gupta T, Gupta SK (2010) ‘ZP domain’ of human zona pellucida glycoprotein-1 binds to human spermatozoa and induces acrosomal exocytosis. Reprod Biol Endocrinol 8:110CrossRefPubMedPubMedCentralGoogle Scholar
  23. Goudet G, Mugnier S, Callebaut I, Monget P (2008) Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol Reprod 78:796–806CrossRefPubMedGoogle Scholar
  24. Greve JM, Wassarman PM (1985) Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J Mol Biol 181:253–264CrossRefPubMedGoogle Scholar
  25. Grützner F, Nixon B, Jones RC (2008) Reproductive biology in egg-laying mammals. Sex Dev 2:115–127CrossRefPubMedGoogle Scholar
  26. Gupta SK (2014) Unraveling the intricacies of mammalian fertilization. Asian J Androl 16:801–802CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gupta SK (2015) Role of zona pellucida glycoproteins during fertilization in humans. Reprod Immunol 108:90–97CrossRefGoogle Scholar
  28. Gupta SK, Bhandari B, Shrestha A, Biswal BK, Palaniappan C, Malhotra SS, Gupta N (2012) Mammalian zona pellucida glycoproteins: structure and function during fertilization. Cell Tissue Res 349:665–678CrossRefPubMedGoogle Scholar
  29. Hamazaki TS, Ichiro I, Yamagami K (1987a) Isolation and partial characterization of a “spawning female-specific substance” in the teleost, Oryzias latipes. J Exp Zool 242:343–349CrossRefGoogle Scholar
  30. Hamazaki TS, Ichiro I, Yamagami K (1987b) Production of a “spawning female-specific substance” in hepatic cells and its accumulation in the ascites of the estrogen-treated adult fish, Oryzias latipes. J Exp Zool 242:325–332CrossRefGoogle Scholar
  31. Hamazaki TS, Nagahama Y, Iuchi I, Yamagami K (1989) A glycoprotein from the liver constitutes the inner layer of the egg envelope (zona pellucid interna) of the fish, Olyzias latipes. Dev Biol 133:101–110CrossRefPubMedGoogle Scholar
  32. Harris JD, Hibler DW, Fontenot GK, Hsu KT, Yurewicz EC, Sacco AG (1994) Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families. DNA Seq 4:361–393CrossRefPubMedGoogle Scholar
  33. Hyllner SJ, Westerlund L, Olsson PE, Schopen A (2001) Cloning of rainbow trout egg envelope proteins: members of a unique group of structural proteins. Biol Reprod 64:805–811CrossRefPubMedGoogle Scholar
  34. Izquierdo-Rico MJ, Jimenez-Movilla M, Llop E, Perez-Oliva AB, Ballesta J, Gutierrez-Gallego R, Jimenez-Cervantes C, Aviles M (2009) Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4. J Proteome Res 8:926–941CrossRefPubMedGoogle Scholar
  35. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y (2000) Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus. Mech Dev 99:139–142CrossRefPubMedGoogle Scholar
  36. LaFleur GJ Jr, Raldúa D, Fabra M, Carnevali O, Denslow N, Wallace RA, Cerdà J (2005) Derivation of major yolk proteins from parental vitellogenins and alternative processing during oocyte maturation in Fundulus heteroclitus. Biol Reprod 73:815–824CrossRefPubMedGoogle Scholar
  37. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lefièvre L, Conner SJ, Salpekar A, Olufowobi O, Ashton P, Pavlovic B, Lenton W, Afnan M, Brewis IA, Monk M, Hughes DC, Barratt CL (2004) Four zona pellucida glycoproteins are expressed in the human. Hum Reprod 19:1580–1586CrossRefPubMedGoogle Scholar
  39. Li CL, Wei QW, Chen XH, Zhou L, Cao H, Gan F, Gui JF (2011) Molecular characterization and expression pattern of three zona pellucida genes in the Chinese sturgeon, Acipenser sinensis. Fish Physiol Biochem 37:471–484CrossRefPubMedGoogle Scholar
  40. Lin Q, Fan S, Zhang Y et al (2016) The seahorse genome and the evolution of its specialized morphology. Nature 540(7633):395–399CrossRefPubMedGoogle Scholar
  41. Lindsay LL, Wallace MA, Hedrick JL (2001) A hatching enzyme substrate in the Xenopus laevis egg envelope is a high molecular weight ZPA homolog. Develop Growth Differ 43:305–313CrossRefGoogle Scholar
  42. Lyons CE, Payette KL, Price JL, Huang RC (1993) Expression and structural analysis of a teleost homolog of a mammalian zona pellucida gene. J Biol Chem 268:21351–21358PubMedGoogle Scholar
  43. Menkhorst E, Selwood L (2008) Vertebrate extracellular preovulatory and postovulatory egg coats. Biol Reprod 79(5):790–797CrossRefPubMedGoogle Scholar
  44. Modig C, Modesto T, Canario A, Cerda J, von Hofsten J, Olsson PE (2006) Molecular characterization and expression pattern of zona pellucida proteins in gilthead seabream (Sparus aurata). Biol Reprod 75:717–725CrossRefPubMedGoogle Scholar
  45. Modig C, Raldúa D, Cerdà J, Olsson PE (2008) Analysis of vitelline envelope synthesis and composition during early oocyte development in gilthead seabream (Sparus aurata). Mol Reprod Dev 8:1351–1360CrossRefGoogle Scholar
  46. Mold DE, Kim IF, Tsai CM, Lee D, Chang CY, Huang RC (2001) Cluster of genes encoding the major egg envelope protein of zebrafish. Mol Reprod Dev 1:4–14CrossRefGoogle Scholar
  47. Monné M, Jovine L (2011) A structural view of egg coat architecture and function in fertilization. Biol Reprod 4:661–669CrossRefGoogle Scholar
  48. Monné M, Han L, Jovine L (2006) Tracking down the ZP domain: from the mammalian zona pellucida to the molluscan vitelline envelope. Semin Reprod Med 24:204–216CrossRefPubMedGoogle Scholar
  49. Murata K, Sasaki T, Yasumasu S, Iuchi I, Enami J, Yasumasu I, Yamagami K (1995) Cloning of cDNAs for the precursor protein of a low-molecular-weight subunit of the inner layer of the egg envelope (chorion) of the fish Oryzias latipes. Dev Biol 167:9–17CrossRefPubMedGoogle Scholar
  50. Murata K, Sugiyama H, Yasumasu S, Iuchi I, Yasumasu I, Yamagami K (1997) Cloning of cDNA and estrogen-induced hepatic gene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion). Proc Natl Acad Sci U S A 94:2050–2055CrossRefPubMedPubMedCentralGoogle Scholar
  51. Murata K, Conte FS, McInnis E, Fong TH, Cherr GN (2014) Identification of the origin and localization of chorion (egg envelope) proteins in an ancient fish, the white sturgeon, Acipenser transmontanus. Biol Reprod 90:132CrossRefPubMedGoogle Scholar
  52. Okumura H, Kohno Y, Iwata Y, Mori H, Aoki N, Sato C, Kitajima K, Nadano D, Matsuda T (2004) A newly identified zona pellucida glycoprotein, ZPD, and dimeric ZP1 of chicken egg envelope are involved in sperm activation on sperm-egg interaction. Biochem J 384:191–199CrossRefPubMedPubMedCentralGoogle Scholar
  53. Sacco AG, Yurewicz EC, Subramanian MG, DeMayo FJ (1981) Zona pellucida composition: species cross reactivity and contraceptive potential of antiserum to a purified pig zona antigen (PPZA). Biol Reprod 25:997–1008CrossRefPubMedGoogle Scholar
  54. Sano K, Kawaguchi M, Yoshikawa M, Iuchi I, Yasumasu S (2010) Evolution of the teleostean zona pellucida gene inferred from the egg envelope protein genes of the Japanese eel, Anguilla japonica. FEBS J 277:4674–4684CrossRefPubMedGoogle Scholar
  55. Sano K, Kawaguchi M, Watanabe S, Nagakura Y, Hiraki T, Yasumasu S (2013) Inferring the evolution of teleostean zp genes based on their sites of expression. J Exp Zool B Mol Dev Evol 320:332–343CrossRefPubMedGoogle Scholar
  56. Schartl M, Walter RB, Shen Y et al (2013) The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits. Nat Genet 45:567–572CrossRefPubMedPubMedCentralGoogle Scholar
  57. Smith J, Paton IR, Hughes DC, Burt DW (2005) Isolation and mapping the chicken zona pellucida genes: an insight into the evolution of orthologous genes in different species. Mol Reprod Dev 70:133–145CrossRefPubMedGoogle Scholar
  58. Spargo SC, Hope RM (2003) Evolution and nomenclature of the zona pellucida gene family. Biol Reprod 68:358–362CrossRefPubMedGoogle Scholar
  59. Stetson I (2015) Four glycoproteins are expressed in the cat zona pellucida. Theriogenology 83:1162–1173CrossRefPubMedGoogle Scholar
  60. Stetson I, Izquierdo-Rico MJ, Moros C, Chevret P, Lorenzo PL, Ballesta J, Rebollar PG, Gutiérrez-Gallego R, Avilés M (2012) Rabbit zona pellucida composition: a molecular, proteomic and phylogenetic approach. J Proteome 75:5920–5935CrossRefGoogle Scholar
  61. Sugiyama H, Yasumasu S, Murata K, Iuchi I, Yamagami K (1998) The third egg envelope subunit in fish: cDNA cloning and analysis, and gene expression. Develop Growth Differ 40:35–45CrossRefGoogle Scholar
  62. Sun Y, Yu H, Zhang Q, Qi J, Zhong Q, Chen Y, Li C (2010) Molecular characterization and expression pattern of two zona pellucida genes in half-smooth tongue sole (Cynoglossus semilaevis). Comp Biochem Physiol B Biochem Mol Biol 155:316–321CrossRefPubMedGoogle Scholar
  63. Tao W, Yuan J, Zhou L, Sun L, Sun Y, Yang S, Li M, Zeng S, Huang B, Wang D (2013) Characterization of gonadal transcriptomes from Nile tilapia (Oreochromis niloticus) reveals differentially expressed genes. PLoS One 8:e63604CrossRefPubMedPubMedCentralGoogle Scholar
  64. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111CrossRefPubMedPubMedCentralGoogle Scholar
  65. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515CrossRefPubMedPubMedCentralGoogle Scholar
  66. Uribe MC, Grier HJ, De la Rosa-Cruz G, Schartl M (2016) The occurrence of spermatozoa in the ovary of the gynogenetic viviparous teleost Poecilia formosa (POECILIIDAE). J Morphol 277:341–350CrossRefPubMedGoogle Scholar
  67. Wang AM (1994) Electron microscopic observations on the formation of chorion (egg envelope) of Oreochromis Mossambicus. Oceanologia Et Limnologia Sinica 25:385–389Google Scholar
  68. Wang H, Gong Z (1999) Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3. Biochim Biophys Acta 1446:156–160CrossRefPubMedGoogle Scholar
  69. Wassarman PM (2008) Zona pellucida glycoproteins. J Biol Chem 36:24285–24289CrossRefGoogle Scholar
  70. Wolf DP, Nishihara T, West DM, Wyrick RE, Hedrick JL (1976) Isolation, physicochemical properties, and macromolecular composition of vitelline and fertilization envelopes from Xenopus laevis eggs. Biochemistry 15:3671–3678CrossRefPubMedGoogle Scholar
  71. Wyrick RE, Nishihara T, Hedrick JL (1974) Fertilization envelope formation by glycoprotein agglutination and block to polyspermy in Xenopus laevis. Fed Proc 33:1453Google Scholar
  72. Xu J, Li JT, Jiang Y, Peng W et al (2016) Genomic basis of adaptive evolution: the survival of Amur ide (Leuciscuswaleckii) in an extremely alkaline environment. Mol Biol Evol 20:msw230Google Scholar
  73. Yuan J, Tao W, Cheng Y, Huang B, Wang D (2014) Genome-wide identification, phylogeny, and gonadal expression of fox genes in Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 40:1239–1252PubMedGoogle Scholar

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© Springer Science+Business Media B.V. 2018

Authors and Affiliations

  1. 1.Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life SciencesSouthwest UniversityChongqingChina
  2. 2.Fisheries CollegeGuangdong Ocean UniversityZhanjiangChina

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