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Domestication is associated with differential expression of pikeperch egg proteins involved in metabolism, immune response and protein folding

Published online by Cambridge University Press:  11 June 2020

J. Nynca*
Affiliation:
Department of Gametes and Embryo Biology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, 10-748Olsztyn, Poland
D. Żarski
Affiliation:
Department of Gametes and Embryo Biology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, 10-748Olsztyn, Poland
J. Bobe
Affiliation:
French National Institute for Agriculture, Food, and Environment (INRAE) | INRAE, Fish Physiology and Genomics Institute (LPGP) UR1037, Campus de Beaulieu, 35042Rennes, France
A. Ciereszko
Affiliation:
Department of Gametes and Embryo Biology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, 10-748Olsztyn, Poland
*
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Abstract

Domestication is a condition in which the breeding, care and feeding of animals are, at least in part, controlled by humans. Information regarding the changes in the protein composition of eggs in response to domestication is very limited. Such data are prerequisite for improvements in the reproduction of domesticated fish. The aim of this study was to examine the impact of domestication on the proteome of pikeperch eggs using two-dimensional differential in-gel electrophoresis. We analysed high-quality eggs from domesticated and wild pikeperch fish to reveal proteins that were presumably only related to the domestication process and not to the quality of eggs. Here, we show that domestication has a profound impact on the protein profile of pikeperch eggs. We identified 66 differentially abundant protein spots, including 27 spots that were more abundant in wild-caught pikeperch eggs and 39 spots that were enriched in eggs collected from domesticated females. Eggs originating from wild-caught females showed higher expression levels of proteins involved in folding, apoptotic process, purine metabolism and immune response, whereas eggs of domesticated females showed higher expression levels of proteins that participated mainly in metabolism. The changes in metabolic proteins in eggs from domesticated females can reflect the adaptation of pikeperch to commercial diets, which have profoundly distinct compositions compared with natural diets. The decrease in the abundance of proteins related to immune response in eggs from the domesticated population suggests that domestication may lead to disturbances in defence mechanisms. In turn, the lower abundance of heat shock proteins in eggs of domesticated fish may indicate their adaptation to stable farming conditions and reduced environmental stressors or their better tolerance of stress from breeding. The proteins identified in this study can increase our knowledge concerning the mechanism of the pikeperch domestication process.

Type
Research Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

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References

Basu, N, Todgham, AE, Ackerman, PA, Bibeau, MR, Nakano, K, Schulte, PM and Iwama, GK 2002. Heat shock protein genes and their functional significance in fish. Gene 295, 173183.CrossRefGoogle ScholarPubMed
Bicskei, B, Taggart, JB, Glover, KA and Bron, JE 2016. Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression. Genetics Selection Evolution 48, 20. doi: 10.1186/s12711-016-0200-6.CrossRefGoogle ScholarPubMed
Bobe, J and Labbé, C 2010. Egg and sperm quality in fish. General and Comparative Endocrinology 165, 535548. doi: 10.1016/j.ygcen.2009.02.011.CrossRefGoogle ScholarPubMed
Bökönyi, S 1969. Archaeological problems of recognizing animal domestication. In The domestication and exploitation of plants and animals (ed. Ucko, PJ and Dimbleby, GW), pp. 219229. Aldine Publishing Company, Chicago, IL, USA.Google Scholar
Boissan, M, Dabernat, S, Peuchant, E, Schlattner, U, Lascu, I and Lacombe, ML 2009. The mammalian Nm23/NDPK family: from metastasis control to cilia movement. Molecular and Cellular Biochemistry 329, 5162. doi: 10.1007/s11010-009-0120-7.Google ScholarPubMed
Bonnet, E, Fostier, A and Bobe, J 2007. Microarray-based analysis of fish egg quality after natural or controlled ovulation. BMC Genomics 8, 55. doi: 10.1186/1471-2164-8-55.CrossRefGoogle ScholarPubMed
Borziak, K, Álvarez-Fernández, A, L Karr, T, Pizzari, T and Dorus, S 2016. The seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication. Scientific Reports 6, 35864. doi: 10.1038/srep35864.Google ScholarPubMed
Bystriansky, JS, Clarke, WC, Alonge, MM, Judd, SM, Schulte, PM and Devlin, RH 2017. Salinity acclimation and advanced parr–smolt transformation in growth-hormone transgenic coho salmon (Oncorhynchus kisutch). Canadian Journal of Zoology 95, 633643. doi: 10.1139/cjz-2016-0201.CrossRefGoogle Scholar
Castets, M-D, Schaerlinger, B, Silvestre, F, Gardeur, J-N, Dieu, M, Corbier, C, Kestemont, P and Fontaine, P 2012. Combined analysis of Perca fluviatilis reproductive performance and oocyte proteomic profile. Theriogenology 78, 432442.CrossRefGoogle ScholarPubMed
Causey, DR, Kim, JH, Stead, DA, Martin, SAM, Devlin, RH and Macqueen, DJ 2019. Proteomic comparison of selective breeding and growth hormone transgenesis in fish: unique pathways to enhanced growth. Journal of Proteomics 192, 114124. doi: 10.1016/j.jprot.2018.08.013.Google ScholarPubMed
Chapman, RW, Reading, BJ and Sullivan, CV 2014. Ovary transcriptome profiling via artificial intelligence reveals a transcriptomic fingerprint predicting egg quality in striped bass, Morone saxatilis. PLoS ONE 9, e96818. doi: 10.1371/journal.pone.0096818.Google ScholarPubMed
Cheon, YP 2016. Adenosine modulates the oocyte developmental competence by exposing stages and synthetic blocking during in vitro maturation. Development & Reproduction. 20, 149155. doi: 10.12717/DR.2016.20.2.149.Google ScholarPubMed
Crespel, A, Helene, R, Erwann, F, Bobe, J and Fauvel, C 2008. Egg quality in domesticated and wild seabass (Dicentrarchus labrax): A proteomic analysis. Cybium 32 (suppl. 2), 205.Google Scholar
Debes, PV, Normandeau, E, Fraser, DJ, Bernatchez, L and Hutchings, JA 2012. Differences in transcription levels among wild, domesticated, and hybrid Atlantic salmon (Salmo salar) from two environments. Molecular Ecology 21, 25742587. doi: 10.1111/j.1365-294X.2012.05567.x.Google ScholarPubMed
Desvignes, T, Fauvel, C and Bobe, J 2011. The nme gene family in zebrafish oogenesis and early development. Naunyn-Schmiedeberg’s Archives of Pharmacology 384, 439449. doi: 10.1007/s00210-011-0619-9.Google ScholarPubMed
Devlin, RH, Sakhrani, D, White, S and Overturf, K 2013. Effects of domestication and growth hormone transgenesis on mRNA profiles in rainbow trout (Oncorhynchus mykiss). Journal of Animal Science 91, 52475258. doi: 10.2527/jas.2013-6612.Google Scholar
Dong, C-H, Yang, S-T, Yang, Z-A, Zhang, L and Gui, J-F 2004. A C-type lectin associated and translocated with cortical granules during oocyte maturation and egg fertilization in fish. Developmental Biology 265, 341354.CrossRefGoogle ScholarPubMed
Douxfils, J, Deprez, M, Mandiki, SN, Milla, S, Henrotte, E, Mathieu, C, Silvestre, F, Vandecan, M, Rougeot, C, Mélard, C, Dieu, M, Raes, M and Kestemont, P 2012. Physiological and proteomic responses to single and repeated hypoxia in juvenile Eurasian perch under domestication - Clues to physiological acclimation and humoral immune modulations. Fish and Shellfish Immunology 33, 11121122. doi: 10.1016/j.fsi.2012.08.013.Google ScholarPubMed
Douxfils, J, Mandiki, SN, Marotte, G, Wang, N, Silvestre, F, Milla, S, Henrotte, E, Vandecan, M, Rougeot, C, Mélard, C and Kestemont, P 2011. Does domestication process affect stress response in juvenile Eurasian perch Perca fluviatilis? Comparative Biochemistry and Physiology - Part A: molecular & Integrative Physiology 159, 9299. doi: 10.1016/j.cbpa.2011.01.021.Google ScholarPubMed
Fontaine, P, Wang, N and Hermelink, B 2015. Broodstock management and control of the reproductive cycle. In Biology and culture of percid fishes (ed. P Kestemont, K Dabrowski and R Summerfelt), pp. 103122. Springer, Dordrecht, Netherlands. doi: 10.1007/978-94-017-7227-3_3.CrossRefGoogle Scholar
Hale, EB 1969. Domestication and the evolution of behavior. In The behaviour of domestic animals, 2nd edition (ed. Hafez, ESE), pp. 2242. Bailliere, Tindall and Cassell, London, UK.Google Scholar
Henrotte, E, Mandiki, RSNM, Prudencio, AT, Vandecan, M, Mélard, C and Kestemont, P 2010. Egg and larval quality, and egg fatty acid composition of Eurasian perch breeders (Perca fluviatilis) fed different dietary DHA/EPA/AA ratios. Aquaculture Research 41, 5361. doi: 10.1111/j.1365-2109.2009.02455.x.Google Scholar
Kamalam, BS, Medale, F and Panserat, S 2017. Utilisation of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies. Aquaculture 467, 327.CrossRefGoogle Scholar
Khendek, A, Chakraborty, A, Roche, J, Ledoré, Y, Personne, A, Policar, T, Żarski, D, Mandiki, R, Kestemont, P, Milla, S and Fontaine, P 2018. Rearing conditions and life history influence the progress of gametogenesis and reproduction performances in pikeperch males and females. Animal 12, 23352346. doi: 10.1017/S1751731118000010.Google ScholarPubMed
Khendek, A, Alix, M, Viot, S, Ledoré, Y, Rousseau, C, Mandik, R, Kestemont, P, Policar, T, Fontaine, P and Milla, S 2017. How does a domestication process modulate oogenesis and reproduction performance in Eurasian perch? Aquaculture 473, 206214. doi: 10.1016/j.aquaculture.2017.02.003.Google Scholar
Li, Y, Li, Y, Cao, X, Jin, X and Jin, T 2017. Pattern recognition receptors in zebrafish provide functional and evolutionary insight into innate immune signaling pathways. Cellular & Molecular Immunology 14, 8089. doi: 10.1038/cmi.2016.50.CrossRefGoogle ScholarPubMed
Molnár, T, Csuvár, A, Benedek, I, Molnár, M and Kabai, P 2018. Domestication affects exploratory behavior of pikeperch (Sander lucioperca L.) during the transition to pelleted food. PLoS ONE 13, e0196118. doi: 10.1371/journal.pone.0196118.Google ScholarPubMed
Nynca, J, Arnold, GJ, Fröhlich, T and Ciereszko, A 2015. Cryopreservation-induced alterations in protein composition of rainbow trout semen. Proteomics 15, 26432654. doi: 10.1002/pmic.201400525.Google ScholarPubMed
Ouatas, T, Selo, M, Sadji, Z, Hourdry, J, Denis, H and Mazabraud, A 1998. Differential expression of nucleoside diphosphate kinases (NDPK/NM23) during Xenopus early development. The International Journal of Developmental Biology 42, 4352.Google ScholarPubMed
Pajares, MA and Pérez-Sala, D 2006. Betaine homocysteine S-methyltransferase: just a regulator of homocysteine metabolism?. Cellular and Molecular Life Sciences 63, 27922803.CrossRefGoogle ScholarPubMed
Palińska-Żarska, K, Woźny, M, Kamaszewski, M, Szudrowicz, H, Brzuzan, P and Żarski, D 2020. Domestication process modifies digestion ability in larvae of Eurasian perch (Perca fluviatilis), a freshwater Teleostei. Scientific Reports 10, 2211. doi: 10.1038/s41598-020-59145-6.CrossRefGoogle Scholar
Price, EO 1999. Behavioral development in animals undergoing domestication. Applied Animal Behaviour Science 65, 245271.CrossRefGoogle Scholar
Roberge, C, Normandeau, E, Einum, S, Guderley, H and Bernatchez, L 2008. Genetic consequences of interbreeding between farmed and wild Atlantic salmon: insights from the transcriptome. Molecular Ecology 17, 314324. doi: 10.1111/j.1365-294X.2007.03438.x.CrossRefGoogle ScholarPubMed
Rocha de Almeida, T, Alix, M, Le Cam, A, Klopp, C, Montfort, J, Toomey, L, Ledoré, Y, Bobe, J, Chardard, D, Schaerlinger, B and Fontaine, P 2019. Domestication may affect the maternal mRNA profile in unfertilized eggs, potentially impacting the embryonic development of Eurasian perch (Perca fluviatilis). PLoS ONE 14, e0226878. doi: 10.1371/journal.pone.0226878.Google Scholar
Roche, J, Żarski, D, Khendek, A, Ben Ammar, I, Broquard, C, Depp, A, Ledoré, Y, Policar, T, Fontaine, P and Milla, S 2018. D1, but not D2, dopamine receptor regulates steroid levels during the final stages of pikeperch gametogenesis. Animal 12, 25872597. doi: 10.1017/S1751731118000824.Google Scholar
Teletchea, F 2019. Fish domestication in aquaculture: reassessment and emerging questions. Cybium 43, 715.Google Scholar
Teletchea, F 2016. Is fish domestication going too fast? Natural Resources 7, 399404.CrossRefGoogle Scholar
Teletchea, F and Fontaine, P 2014. Levels of domestication in fish: implications for the sustainable future of aquaculture. Fish and Fisheries 15, 181195. doi: 10.1111/faf.12006.Google Scholar
Tymchuk, W, Sakhrani, D and Devlin, R 2009. Domestication causes large-scale effects on gene expression in rainbow trout: analysis of muscle, liver and brain transcriptomes. General and Comparative Endocrinology 164, 175183. doi: 10.1016/j.ygcen.2009.05.015.Google ScholarPubMed
Vogel, C and Marcotte, EM 2012. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews Genetics 13, 227232. doi: 10.1038/nrg3185.CrossRefGoogle ScholarPubMed
Yilmaz, M and Ablak, O 2003. The feeding behavior of pike perch (Sander lucioperca (L. 1758)) living in Hirfanli dam lake. The Turkish Journal of Veterinary and Animal Sciences 27, 11591165.Google Scholar
Żarski, D, Fontaine, P, Roche, J, Alix, M, Blecha, M, Broquard, C, Król, J and Milla, S 2019. Time of response to hormonal treatment but not the type of a spawning agent affects the reproductive effectiveness in domesticated pikeperch, Sander lucioperca. Aquaculture 503, 527536. doi: 10.1016/j.aquaculture.2019.01.042.CrossRefGoogle Scholar
Żarski, D, Kucharczyk, D, Targońska, K, Palińska, K, Kupren, K, Fontaine, P and Kestemont, P 2012. A new classification of pre-ovulatory oocyte maturation stages in pikeperch, Sander lucioperca (L.), and its application during artificial reproduction. Aquaculture Research 43, 713721.CrossRefGoogle Scholar
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