Transfer of the <i>zp3a</i> gene results in changes in egg adhesiveness and buoyancy in transgenic zebrafish

Yu-Qing Cao; Yong-Xin Wang; Yan Zhao; Jia Zhang; Xian He; Ping Xie; Jun Chen; Yu-Hua Sun

doi:10.24272/j.issn.2095-8137.2022.330

Article Contents

Article Navigation > Zoological Research > 2023 > In Press

Yu-Qing Cao, Yong-Xin Wang, Yan Zhao, Jia Zhang, Xian He, Ping Xie, Jun Chen, Yu-Hua Sun. Transfer of the zp3a gene results in changes in egg adhesiveness and buoyancy in transgenic zebrafish. Zoological Research, 2023, 44(2): 259-268. doi: 10.24272/j.issn.2095-8137.2022.330

Citation:

Yu-Qing Cao, Yong-Xin Wang, Yan Zhao, Jia Zhang, Xian He, Ping Xie, Jun Chen, Yu-Hua Sun. Transfer of the zp3a gene results in changes in egg adhesiveness and buoyancy in transgenic zebrafish. Zoological Research, 2023, 44(2): 259-268. doi: 10.24272/j.issn.2095-8137.2022.330

Citation:

PDF( 9419 KB)

Transfer of the zp3a gene results in changes in egg adhesiveness and buoyancy in transgenic zebrafish

doi: 10.24272/j.issn.2095-8137.2022.330

Yu-Qing Cao^{1, 3},
Yong-Xin Wang^{1, 3},
Yan Zhao^{3, 4},
Jia Zhang^{3, 4},
Xian He^{1, 3},
Ping Xie⁴,
Jun Chen^{4
,
,},
Yu-Hua Sun^{1, 2, 3
,
,}

1.
Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei 430072, China
2.
Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100049, China
3.
University of Chinese Academy of Sciences, Beijing 100049, China
4.
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei 430072, China

Raw data were submitted to the NCBI Sequence Read Archive (SRA) database (BioProjectID PRJNA910672), GSA database (PRJCA013771), and Science Data Bank database (DOI:10.57760/sciencedb.j00139.00044, DOI:10.57760/sciencedb.06900).
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
Y.Q.C., Y.X.W., and X.H. from Sun Lab performed most experiments. Y.Z. and J.Z. performed the TEM experiments. P.X., J.C., and Y.H.S. supervised the work. Y.H.S. provided the facilities for the work and wrote the manuscript. All authors read and approved the final version of the manuscript.

Funds: This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31000000)

More Information

Corresponding author: E-mail: sunyh@ihb.ac.cn; chenjun@ihb.ac.cn
Received Date: 2022-11-30
Accepted Date: 2023-01-13

Published Online: 2023-01-13

Abstract

Abstract

Reproductive strategies and spawning habits play key roles in the evolution of endemic East Asian cyprinids. However, the molecular mechanisms underlying the regulation of spawning habits are not well understood. We recently identified zona pellucida (Zp) as the top differentially expressed protein between East Asian cyprinids that produce adhesive and semi-buoyant eggs, suggesting that Zp protein may play important roles in the regulation of egg type. In this work, we generated transgenic zebrafish in which oocyte-specific expression of zp genes from rare minnow (Gobiocypris rarus), an East Asian cyprinid laying adhesive eggs, was driven by a zebrafish zp3.2 gene promoter. We found that the transgenic eggs obtained partial adhesiveness and exhibited alteration in hydration and buoyancy. Abnormal metabolism of vitellogenin (VTG) may contribute to enhanced hydration and/or buoyancy. Our work shows that expression of the exogenous zp3a gene from an adhesive-egg producing fish is sufficient to induce changes in both egg adhesiveness and buoyancy in zebrafish, emphasizing the important role of zp genes in the regulation of spawning habits. Our results thus provide new insights into how endemic East Asian cyprinids may have adapted to the Yangtze river-lake system via changes in spawning habits.
- Zona pellucida protein,
- Adhesive,
- Buoyancy,
- Hydration,
- Egg envelope

FullText(HTML)

References(38)

References

[1]	Averianova LA, Balabanova LA, Son OM, et al. 2020. Production of vitamin B2 (riboflavin) by microorganisms: an overview. Frontiers in Bioengineering and Biotechnology, 8: 570828. doi: 10.3389/fbioe.2020.570828
[2]	Baras E, Arifin OZ, Slembrouck J, et al. 2018. Oil globule size in fish eggs: a matter of biome and reproductive strategy. Fish and Fisheries, 19(6): 996−1002. doi: 10.1111/faf.12307
[3]	Boja ES, Hoodbhoy T, Fales HM, et al. 2003. Structural characterization of native mouse zona pellucida proteins using mass spectrometry. Journal of Biological Chemistry, 278(36): 34189−34202. doi: 10.1074/jbc.M304026200
[4]	Bonsignorio D, Perego L, Del Giacco L, et al. 1996. Structure and macromolecular composition of the zebrafish egg chorion. Zygote, 4(2): 101−108. doi: 10.1017/S0967199400002975
[5]	Cao LX, Huang Q, Wu ZC, et al. 2016. Neofunctionalization of zona pellucida proteins enhances freeze-prevention in the eggs of antarctic notothenioids. Nature Communications, 7: 12987. doi: 10.1038/ncomms12987
[6]	Cerda J, Fabra M, Raldua D. 2007. Physiological and molecular basis of fish oocyte hydration. In: Babin PJ, et al. (eds. ). The Fish Oocyte: From Basic Studies to Biotechnological Applications. Amsterdam, Netherlands: Springer Press, 349–396.
[7]	Chang YS, Wang YW, Huang FL. 2002. Cross-linking of ZP2 and ZP3 by Transglutaminase is required for the formation of the outer layer of fertilization envelope of carp egg. Molecular Reproduction and Development, 63(2): 237−244. doi: 10.1002/mrd.10174
[8]	Chen F, Smith C, Wang YK, et al. 2021. The evolution of alternative buoyancy mechanisms in freshwater fish eggs. Frontiers in Ecology and Evolution, 9: 736718. doi: 10.3389/fevo.2021.736718
[9]	Chen F, Wang YK, He J, et al. 2022. Molecular mechanisms of spawning habits for the adaptive radiation of endemic East Asian cyprinid fishes. Research, 2022: 9827986.
[10]	Dutta A, Sinha DK. 2017. Zebrafish lipid droplets regulate embryonic ATP homeostasis to power early development. Open Biology, 7(7): 170063. doi: 10.1098/rsob.170063
[11]	Esmaeili HR, Johal MS. 2005. Ultrastructural features of the egg envelope of silver carp, Hypophthalmichthys molitrix (osteichthyes, cyprinidae). Environmental Biology of Fishes, 72(4): 373−377. doi: 10.1007/s10641-004-2589-y
[12]	Fabra M, Raldúa D, Power DM, Deen PMT, Cerdà J. 2005. Marine fish egg hydration is aquaporin-mediated. Science, 307(5709): 545. doi: 10.1126/science.1106305
[13]	Feng CG, Wang K, Xu WJ, et al. 2022. Monsoon boosted radiation of the endemic East Asian carps. Science China Life Sciences,doi: 10.1007/s11427-022-2141-1.
[14]	Fraher D, Sanigorski A, Mellett NA, et al. 2016. Zebrafish embryonic lipidomic analysis reveals that the yolk cell is metabolically active in processing lipid. Cell Reports, 14(6): 1317−1329. doi: 10.1016/j.celrep.2016.01.016
[15]	Galliano M, Minchiotti L, Campagnoli M, et al. 2003. Structural and biochemical characterization of a new type of lectin isolated from carp eggs. Biochemical Journal, 376(2): 433−440. doi: 10.1042/bj20030413
[16]	Gao LL, Zhou CX, Zhang XL, et al. 2017. ZP3 is required for germinal vesicle breakdown in mouse oocyte meiosis. Scientific Reports, 7: 41272. doi: 10.1038/srep41272
[17]	Hachicho N, Reithel S, Miltner A, et al. 2015. Body mass parameters, lipid profiles and protein contents of zebrafish embryos and effects of 2, 4-dinitrophenol exposure. PLoS One, 10(8): e0134755. doi: 10.1371/journal.pone.0134755
[18]	Hu XD, Li HR, Lin YS, et al. 2022. Genomic deciphering of sex determination and unique immune system of a potential model species rare minnow (Gobiocypris rarus). Science Advances, 8(5): eabl7253. doi: 10.1126/sciadv.abl7253
[19]	Jovine L, Qi HY, Williams Z, et al. 2002. The ZP domain is a conserved module for polymerization of extracellular proteins. Nature Cell Biology, 4(6): 457−461. doi: 10.1038/ncb802
[20]	Kawakami K, Takeda H, Kawakami N, et al. 2004. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Developmental Cell, 7(1): 133−144. doi: 10.1016/j.devcel.2004.06.005
[21]	Kong XH, Wang XZ, Gan XN, et al. 2007. The c-myc coding DNA sequences of cyprinids (Teleostei: Cypriniformes): implications for phylogeny. Chinese Science Bulletin, 52(11): 1491−1500. doi: 10.1007/s11434-007-0216-y
[22]	Liu XJ, Wang H, Gong ZY. 2006. Tandem-repeated zebrafish Zp3 genes possess oocyte-specific promoters and are insensitive to estrogen induction. Biology of Reproduction, 74(6): 1016−1025. doi: 10.1095/biolreprod.105.049403
[23]	Mansour N, Lahnsteiner F, Patzner RA. 2009. Physiological and biochemical investigations on egg stickiness in common carp. Animal Reproduction Science, 114(1–3): 256–268.
[24]	Marques DA, Meier JI, Seehausen O. 2019. A combinatorial view on speciation and adaptive radiation. Trends in Ecology & Evolution, 34(6): 531−544.
[25]	McGee MD, Borstein SR, Meier JI, et al. 2020. The ecological and genomic basis of explosive adaptive radiation. Nature, 586(7827): 75−79. doi: 10.1038/s41586-020-2652-7
[26]	Murray DS, Bain MM, Adams CE. 2013. Adhesion mechanisms in European whitefish Coregonus lavaretus eggs: is this a survival mechanism for high-energy spawning grounds?. Journal of Fish Biology, 83(5): 1221−1233. doi: 10.1111/jfb.12218
[27]	Niksirat H, Andersson L, Golpour A, et al. 2017. Quantification of egg proteome changes during fertilization in sterlet Acipenser ruthenus. Biochemical and Biophysical Research Communications, 490(2): 189–193.
[28]	Niksirat H, Levander F, Kouba A, et al. 2020. Proteomic changes after fertilization and before first cleavage in rainbow trout Oncorhynchus mykiss. Aquaculture, 520: 734951.
[29]	Riehl R, Patzner RA. 1998. Minireview: the modes of egg attachment in teleost fishes. Italian Journal of Zoology, 65(sup1): 415−420. doi: 10.1080/11250009809386857
[30]	Rizzo E, Sato Y, Barreto BP, et al. 2002. Adhesiveness and surface patterns of eggs in neotropical freshwater teleosts. Journal of Fish Biology, 61(3): 615−632. doi: 10.1111/j.1095-8649.2002.tb00900.x
[31]	Sano K, Kawaguchi M, Katano K, et al. 2017. Comparison of egg envelope thickness in teleosts and its relationship to the sites of ZP protein synthesis. Journal of Experimental Zoology Part B:Molecular and Developmental Evolution, 328(3): 240−258. doi: 10.1002/jez.b.22729
[32]	Sun XJ, Wang PX. 2005. How old is the Asian monsoon system?——Palaeobotanical records from China. Palaeogeography, Palaeoclimatology, Palaeoecology, 222(3–4): 181–222.
[33]	Tao TQ, He T, Wang XR, et al. 2019. Metabolic profiling analysis of patients with coronary heart disease undergoing Xuefu Zhuyu decoction treatment. Frontiers in Pharmacology, 10: 985. doi: 10.3389/fphar.2019.00985
[34]	Tao WJ, Zou M, Wang XZ, et al. 2010. Phylogenomic analysis resolves the formerly intractable adaptive diversification of the Endemic clade of East Asian cyprinidae (Cypriniformes). PLoS One, 5(10): e13508. doi: 10.1371/journal.pone.0013508
[35]	Wang H, Gong ZY. 1999. Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3. Biochimica et Biophysica Acta, 1446: 156−160. doi: 10.1016/S0167-4781(99)00066-4
[36]	Wang N, Wu FX. 2015. New Oligocene cyprinid in the central Tibetan Plateau documents the pre-uplift tropical lowlands. Ichthyological Research, 62(3): 274−285. doi: 10.1007/s10228-014-0438-3
[37]	Wang YK, Chen F, He J, et al. 2022. Comparative ultrastructure and proteomics of two economic species (common carp and grass carp) egg envelope. Aquaculture, 546: 737276. doi: 10.1016/j.aquaculture.2021.737276
[38]	Zheng HB. 2015. Birth of the Yangtze River: age and tectonic-geomorphic implications. National Science Review, 2(4): 438−453. doi: 10.1093/nsr/nwv063