Abstract
Annual killifish are freshwater teleosts that have a short lifespan and inhabit shallow temporal ponds in regions of the Americas and Africa. During the dry season, adults die while embryos survive by being buried in the bottom mud and hatching during the next rainy season. Juveniles reach sexual maturity within few weeks. Hence, species survival is entirely embryo-dependent, and killifish exhibit a set of unique developmental features. Epiboly is temporarily and spatially detached from axis formation (dispersion-reaggregation phase) and embryos undergo reversible arrests or diapauses. Furthermore, the egg envelope is a notably strong structure and protects the embryos during the long development that they undergo. The present study reports the identification and characterization of two egg envelope proteins and the involved genes, achzpL and achzpH, both expressed in the liver under hormone regulation. This study’s results help to elucidate the function of the embryo egg envelope. Moreover, the oestrogen-regulated liver expression of these genes allows us to suggest components of the annual killifish egg envelope as possible biomarkers to monitor water contamination.
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Altschul S, Madden T, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3340
Arezo MJ, D’Alessandro S, Papa N, de Sá RO, Berois N (2007) Sex differentiation pattern in the annual fish Austrolebias charrua (Cyprinodontiformes: Rivulidae). Tissue Cell 39:89–98. https://doi.org/10.1111/j.0022-1112.2005.00688.x
Arezo MJ, Papa N, Guttierrez V, García G, Berois N (2014) Sex determination in annual fishes: searching for the master sex-determining gene in Austrolebias charrua (Cyprinodontiformes, Rivulidae). Genet Mol Biol 37:364–374
Arukwe A, Goksøyr A (2003) Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: Oogenetic, population, and evolutionary implications of endocrine disruption. Comp Hepatol 2:4. https://doi.org/10.1186/1476-5926-2-4
Arukwe A, Knudsen FR, Goksøyr A (1997) Fish zona radiata (egg shell) protein: a sensitive biomarker for environmental estrogens. Environ Health Perspect 105:418–422
Arukwe A, Celius T, Walther BT, Goksøyr A (2000) Effects of xenoestrogen treatment on zona radiata protein and vitellogenin expression in Atlantic salmon (Salmo salar). Aquat Toxicol 49:159–170. https://doi.org/10.1016/S0166-445X(99)00083-1
Barrallo A, Gonzalez-Sarmiento R, Garcia-Isidoro M, Cidad P, Porteros A, Rodriguez R (1999) Differential brain expression of a new beta-actin gene from zebrafish (Danio rerio). Eur J Neurosci 11:369–372
Berois N, Arezo MJ, Papa NG (2011) Gamete interaction in teleost fish: the egg envelope. Basic studies and perspectives as environmental biomonitor. Biol Res 44(2):119–124. https://doi.org/10.4067/S0716-97602011000200002
Berois N, Arezo MJ, Papa NG, Clivio GA (2012) Annual fish: developmental adaptations for an extreme environment. Wiley Interdiscip Rev Dev Biol 1:595–602. https://doi.org/10.1002/wdev.39
Bettinetti R, Provini A (2002) Toxicity of 4-nonylphenol to Tubifex tubifex and Chironomus riparius in 28-day whole-sediment tests. Ecotoxicol Environ Saf 53:113–121
Bettinetti R, Cuccato D, Galassi S, Provini A (2002) Toxicity of 4-nonylphenol in spiked sediment to three populations of Chironomus riparius. Chemosphere 46:201–207
Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258
Blažek R, Polačik M, Reichard M (2013) Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo 4:24. https://doi.org/10.1186/2041-9139-4-24
Chen X, Li VW, Yu RM, Cheng SH (2008) Choriogenin mRNA as a sensitive molecular biomarker for estrogenic chemicals in developing brackish medaka (Oryzias melastigma). Ecotoxicol Environ Saf 71:200–208. https://doi.org/10.1016/j.ecoenv.2007.10.005
Cheng J, Baldi P (2005) Three-stage prediction of protein Beta-sheets by neural networks, alignments, and graph algorithms. Bioinformatics 21:i75–i84
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 126:347–352. https://doi.org/10.1093/humrep/deh835
Costa WEJM (2006) The south American annual killifish genus Austrolebias (Teleostei: Cyprinodontiformes: Rivulidae): phylogenetic relationships, descriptive morphology and taxonomic revision. Zootaxa 1213:1–162. https://doi.org/10.11646/zootaxa.1067.1.1
Costa WJEM, Cheffe MM (2001) Three new annual fishes of the genus Austrolebias from the Laguna dos Patos system, southern Brazil, and a rediscription of A. adloffi (AHL) (Cyprinodontiformes: rivulidae). Comun Mus Ciênc Tecnol PUCRS Sér Zool Porto Alegre 14:179–200
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 Dev 75:1217–1728. https://doi.org/10.1002/mrd.20857
Furness AI (2015) The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause. Biol Rev Camb Philos Soc 91:796–812. https://doi.org/10.1111/brv.12194
García G, Alvarez-Valin F, Gomez N (2002) Mitochondrial genes: signals and noise in phylogenetic reconstruction within killifish genus Cynolebias (Cyprinodontiformes, Rivulidae). Biol J Linn Soc 76:49–59. https://doi.org/10.1111/j.1095-8312.2002.tb01713.x
Han L, Monné M, Okumura H, Schwend T, Cherry AL, Flot D, Matsuda T, Jovine L (2010) Insights into oocyte envelope assembly and egg-sperm interaction from the X-ray structure of full-length ZP3. Cell 143:404–415. https://doi.org/10.1016/j.cell.2010.09.041
Johnson KM, Lema SC (2017) Temporal patterns of induction and recovery of biomarker transcriptional responses to 4-Nonylphenol and 17β-estradiol in the estuarine arrow goby, Clevelandia ios. Environ Toxicol 32:1513–1529. https://doi.org/10.1002/tox.22371
Jovine L, Costel C, Litscher E, Wassarman P (2005) Zona Pellucida Domain Proteins. Annu Rev Biochem 74:83–114. https://doi.org/10.1146/annurev.biochem.74.082803.133039
Knoebl I, Hemmer MJ, Denslow ND (2004) Induction of zona radiata and vitellogenin genes in estradiol and nonylphenol exposed male sheepshead minnows (Cyprinodon variegatus). Mar Environ Res 58:547–551. https://doi.org/10.1016/j.marenvres.2004.03.043
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lee C, Jeon SH, Na J, Choi Y, Park K (2002) Sensitivities of mRNA expression of vitellogenin, choriogenin and estrogen receptor by estrogenic chemicals in medaka, Oryzias latipes. J Health Sci 48:441–445
Litscher ES, Wassarman PM (2007) Egg extracellular coat proteins: from fish to mammals. Histol Histopathol 22:337–347. https://doi.org/10.14670/HH-22.337
Litscher ES, Wassarman PM (2018) The fish Egg's zona Pellucida. Curr Top Dev Biol 130:275–305. https://doi.org/10.1016/bs.ctdb.2018.01.002
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Loureiro M, Borthagaray A, Hernandez D, Duarte A, Pinelli V, Arim M (2016) Austrolebias in space: scaling from ponds to biogeographical regions. In: Berois N, Garcia G, de Sá RO (eds) Annual fishes: life history strategy, diversity and evolution, 1st edn. CRC Press Taylor and Francis, Boca Raton, pp 111–132
Mäenpää K, Kukkonen JVK (2006) Bioaccumulation and toxicity of 4-nonylphenol (4-NP) and 4-(2-dodecyl)-benzene sulfonate (LAS) in Lumbriculus variegatus (Oligochaeta) and Chironomus riparius (Insecta). Aquat Toxicol 77:329–338. https://doi.org/10.1016/j.aquatox.2006.01.002
Matthiessen P, Wheeler JR, Weltje L (2018) A review of the evidence for endocrine disrupting effects of current-use chemicals on wildlife populations. Crit Rev Toxicol 48:195–216. https://doi.org/10.1080/10408444.2017.1397099
McCurley AT, Callard GV (2008) Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol 9:102. https://doi.org/10.1186/1471-2199-9-102
Monné M, Jovine L (2011) A structural view of egg coat architecture and function in fertilization. Biol Reprod 4:661–669. https://doi.org/10.1095/biolreprod.111.092098
Nei M, Kumar S (2000) Molecular evolution and Phylogenetics. In: Thomas RH (ed) Heredity, vol 86, 1st edn. Oxford University Press, New York, pp 385–386. https://doi.org/10.1046/j.1365-2540.2001.0923a.x
Papa NG, Clivio GA, Montagne J (2016) Husbandry, reproduction, and embryo culture of annual fishes under laboratory conditions. In: Berois N, Garcia G, de Sá RO (eds) Annual fishes: life history strategy, diversity and evolution, 1st edn. CRC Press Taylor and Francis, Boca Raton, pp 99–110
Peters N (1963) Embryonale Anpassungen oviparer Zahnkarpfen aus periodisch austrocknenden Gewässern. Int Rev Gesamten Hydrobiol 48:257–313. https://doi.org/10.1002/iroh.19630480204
Podrabsky JE, Carpenter JF, Hand SC (2001) Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. Am J Phys Regul Integr Comp Phys 280:R123–R131. https://doi.org/10.1152/ajpregu.2001.280.1.R123
Reichwald K, Petzold A, Koch P, Downie BR, Hartmann N, Pietsch S, Baumgart M, Chalopin D, Felder M, Bens M, Sahm A, Szafranski K, Taudien S, Groth M, Arisi I, Weise A, Bhatt SS, Sharma V, Kraus JM, Schmid F, Priebe S, Liehr T, Görlach M, Than ME, Hiller M, Kestler HA, Volff JN, Schartl M, Cellerino A, Englert C, Platzer M (2015) Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell 163:1527–1538. https://doi.org/10.1016/j.cell.2015.10.071
Rhee JS, Kang HS, Raisuddin S, Hwang DS, Han J, Kim RO, Seo JS, Lee YM, Park GS, Lee SJ, Lee JS (2009) Endocrine disruptors modulate expression of hepatic choriogenin genes in the hermaphroditic fish, Kryptolebias marmoratus. Comp Biochem Physiol C Toxicol Pharmacol 150:170–178. https://doi.org/10.1016/j.cbpc.2009.04.006
Riggs CL, Summers A, Warren DE, Nilsson GE, Lefevre S, Dowd WW, Milton S, Podrabsky JE (2018) Small non-coding RNA expression and vertebrate anoxia tolerance. Front Genet 9:230. https://doi.org/10.3389/fgene.2018.00230
Rutledge RG, Côté C (2003) Mathematics of quantitative kinetic PCR and the application of standard curves. Nucleic Acids Res 31:e93 993
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sayed AE, Hamed HS (2017) Induction of apoptosis and DNA damage by 4-nonylphenol in African catfish (Clarias gariepinus) and the antioxidant role of Cydonia oblonga. Ecotoxicol Environ Saf 139:97–101. https://doi.org/10.1016/j.ecoenv.2017.01.024
Sayed AEH, Ismail RFK (2017) Endocrine disruption, oxidative stress, and testicular damage induced by 4-nonylphenol in Clarias gariepinus: the protective role of Cydonia oblonga. Fish Physiol Biochem 43:1095–1104. https://doi.org/10.1007/s10695-017-0355-2
Sharma M, Chadha P (2018) Toxicity of non-ionic surfactant 4-nonylphenol an endocrine disruptor: a review. Int J Fish Aquat 6:190–197
Shu L, Suter MJ, Räsänen K (2015) Evolution of egg coats: linking molecular biology and ecology. Mol Ecol 24:4052–4073. https://doi.org/10.1111/mec.13283
Snyder SA, Keith TL, Naylor CG, Staples CA, Giesy JP (2001) Identification and quantitation method for nonylphenol and lower oligomer nonylphenol ethoxylates in fish tissues. Environ Toxicol Chem 20:1870–1873
Soares A, Guieysse B, Jefferson B, Cartmell E (2008) Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ Int 34:1033–1049. https://doi.org/10.1016/j.envint.2008.01.004
Spargo SC, Hope RM (2003) Evolution and nomenclature of the zona pellucida gene family. Biol Reprod 68:358–362. https://doi.org/10.1095/biolreprod.102.008086
Taphorn DC, Thomerson JE (1978) A revision of the South American cyprinodont fishes of the genera Rachovia and Austrofundulus, with the description of a new genus. Acta Biol Venez 9:377–452
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
UNESCO (1976) The MAB Programme. UNESCO = MAB Biosphere Reserves Directory. IOP Publishing PhysicWeb. http://www.unesco.org/mabdb/br/brdir/directory/biores.asp?code=URU+01&mode=all
Volcan MV, Lanés LEK (2018) Brazilian killifishes risk extinction. Science 361:340–341. https://doi.org/10.1126/science.aau5930
Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343 http://www.jstor.org/stable/3882637
Wang H, Gong Z (1999) Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3. Biochim Biophys Acta 1446:156–160
Wassarman PM, Litscher ES (2016) A Bespoke Coat for Eggs: Getting Ready for Fertilization. Curr Top Dev Biol 117:539–552. https://doi.org/10.1016/bs.ctdb.2015.10.018
Wourms JP (1972a) The developmental biology of annual fishes III. Preembryonic and embryonic diapause of variable duration in the eggs of annual fishes. J Exp Zool 182:389–414. https://doi.org/10.1002/jez.1401820310
Wourms JP (1972c) Developmental biology of annual fishes I. Stages in the normal development of Austrofundulus myersi dahl. J Exp Zool 182:143–168. https://doi.org/10.1002/jez.1401820202
Yu R, Wong M, Kong R, Wu R, Cheng S (2006) Induction of hepatic choriogenin mRNA expression in male marine medaka: a highly sensitive biomarker for environmental estrogens. Aquat Toxicol 77:348–358. https://doi.org/10.1016/j.aquatox.2006.01.003
Zielinska D, Gnad F, Wisniewski J, Mann M (2010) Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141:897–907. https://doi.org/10.1016/j.cell.2010.04.012
Acknowledgements
The authors wish to thank Dr. Gonzalo Greiff form Instituto Pasteur de Montevideo for kindly collaboration during primer design, RNA quantification and qPCR and Mrs. Barbara Hunter for English assistance. The original findings presented in this paper were part of a PEDECIBA (Programa de Desarrollo Ciencias Básicas) MSc. thesis by N Papa. Financial support was provided by Agencia Nacional de Investigación e Innovación (ANII), PEDECIBA, Comisión Sectorial de Investigación Científica (CSIC) and Facultad de Ciencias - Universidad de la República, Montevideo, Uruguay.
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Animals used in this study were manipulated according to an ethic protocol approved by the animal experimentation committee from the Universidad de la República, CHEA (Comisión Honoraria de Experimentación Animal, protocol code Facultad de Ciencias Exp240011–001205-16).
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Fig. 7
Structural model for AchzpH. The crystal structure of sperm receptor ZP3 (PDB entry 3NK3) was used as a template to build AchzpH homology model by SWISS-MODEL server. (PNG 186 kb)
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Papa, N.G., Chalar, C., Berois, N. et al. Annual killifish: an approach to the choriogenins of Austrolebias charrua egg envelope. Environ Biol Fish 102, 829–844 (2019). https://doi.org/10.1007/s10641-019-00861-y
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DOI: https://doi.org/10.1007/s10641-019-00861-y