Early fasting does not impact gonadal size nor vasa gene expression in the European seabass Dicentrarchus labrax.
Primordial germ cells
Sex determination
Sex differentiation
Starvation
Journal
Fish physiology and biochemistry
ISSN: 1573-5168
Titre abrégé: Fish Physiol Biochem
Pays: Netherlands
ID NLM: 100955049
Informations de publication
Date de publication:
28 Aug 2024
28 Aug 2024
Historique:
received:
03
05
2024
accepted:
10
08
2024
medline:
28
8
2024
pubmed:
28
8
2024
entrez:
28
8
2024
Statut:
aheadofprint
Résumé
Primordial germ cells (PGCs) play a crucial role in sexual development in fish, with recent studies revealing their influence on sexual fate. Notably, PGC number at specific developmental stages can determine whether an individual develops as male or female. Temperature was shown to impact PGC proliferation and the subsequent phenotypic sex in some fish species. Here, we aimed at testing the role of food deprivation on gonad development in the European seabass Dicentrarchus labrax, a species displaying a polygenic sex determination system with an environmental influence. We subjected larvae to two periods of starvation to investigate whether restricting growth affects both gonadal size and vasa gene expression. We first confirmed by immunohistochemistry that Vasa was indeed a marker of PGCs in the European seabass, as in other fish species. We also showed that vasa correlated positively with fish size, confirming that it could be used as a marker of feminization. However, starvation did not show any significant effects on vasa expression nor on gonadal size. It is hypothesized that evolutionary mechanisms likely safeguard PGCs against environmental stressors to ensure reproductive success. Further research is needed to elucidate the intricate interplay between environmental cues, PGC biology, and sexual differentiation in fish.
Identifiants
pubmed: 39196454
doi: 10.1007/s10695-024-01395-6
pii: 10.1007/s10695-024-01395-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : European Maritime and Fisheries Fund
ID : 4320175237
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Adolfi MC, Fischer P, Herpin A et al (2019) Increase of cortisol levels after temperature stress activates dmrt1a causing female-to-male sex reversal and reduced germ cell number in medaka. Mol Reprod Dev 86:1405–1417. https://doi.org/10.1002/mrd.23177
doi: 10.1002/mrd.23177
pubmed: 31140678
Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Grothendieck G, Green P, Bolker MB (2015) Package ‘lme4’. convergence, 12(1):2
Blázquez M, González A, Mylonas CC, Piferrer F (2011) Cloning and sequence analysis of a vasa homolog in the European sea bass (Dicentrarchus labrax): tissue distribution and mRNA expression levels during early development and sex differentiation. Gen Comp Endocrinol 170:322–333. https://doi.org/10.1016/j.ygcen.2010.10.007
doi: 10.1016/j.ygcen.2010.10.007
pubmed: 20955711
Braat AK, Zandbergen T, Van De Water S (1999) Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev Dyn 216:153–167
doi: 10.1002/(SICI)1097-0177(199910)216:2<153::AID-DVDY6>3.0.CO;2-1
pubmed: 10536055
Clota F, Goikoetxea A, Vergnet A et al (2024) Post-larval exposure to warm temperature enhances female ratio, while starvation and photoperiod do not: the case of European seabass. Dicentrarchus Labrax Aquaculture 586:740758. https://doi.org/10.1016/j.aquaculture.2024.740758
doi: 10.1016/j.aquaculture.2024.740758
Díaz N, Ribas L, Piferrer F (2013) The relationship between growth and sex differentiation in the European sea bass (Dicentrarchus labrax). Aquaculture 408–409:191–202. https://doi.org/10.1016/j.aquaculture.2013.05.032
doi: 10.1016/j.aquaculture.2013.05.032
Duangkaew R, Jangprai A, Ichida K et al (2019) Characterization and expression of a vasa homolog in the gonads and primordial germ cells of the striped catfish (Pangasianodon hypophthalmus). Theriogenology 131:61–71. https://doi.org/10.1016/j.theriogenology.2019.01.022
doi: 10.1016/j.theriogenology.2019.01.022
pubmed: 30947076
Faggion S, Vandeputte M, Vergnet A et al (2021) Sex dimorphism in European sea bass (Dicentrarchus labrax L): new insights into sex-related growth patterns during very early life stages. PLOS ONE 16:e0239791. https://doi.org/10.1371/journal.pone.0239791
doi: 10.1371/journal.pone.0239791
pubmed: 33886551
pmcid: 8061996
Fujimoto T, Nishimura T, Goto-Kazeto R et al (2010) Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish. Proc Natl Acad Sci 107:17211–17216. https://doi.org/10.1073/pnas.1007032107
doi: 10.1073/pnas.1007032107
pubmed: 20855617
pmcid: 2951417
Gabe M (1968) Techniques histologiques. In: Masson et Cie eds, Paris p 1113
Geffroy B (2022) Energy as the cornerstone of environmentally driven sex allocation. Trends Endocrinol Metab 33:670–679. https://doi.org/10.1016/j.tem.2022.07.002
doi: 10.1016/j.tem.2022.07.002
pubmed: 35934660
Geffroy B, Wedekind C (2020) Effects of global warming on sex ratios in fishes. J Fish Biol 97:596–606. https://doi.org/10.1111/jfb.14429
doi: 10.1111/jfb.14429
pubmed: 32524610
Geffroy B, Besson M, Sánchez-Baizán N, et al (2021) Unraveling the genotype by environment interaction in a thermosensitive fish with a polygenic sex determination system. Proc Natl Acad Sci 118 https://doi.org/10.1073/pnas.2112660118
Gleason RJ, Anand A, Kai T, Chen X (2018) Protecting and diversifying the germline. Genetics 208:435–471. https://doi.org/10.1534/genetics.117.300208
doi: 10.1534/genetics.117.300208
pubmed: 29378808
pmcid: 5788515
Goto R, Saito T, Takeda T et al (2012) Germ cells are not the primary factor for sexual fate determination in goldfish. Dev Biol 370:98–109. https://doi.org/10.1016/j.ydbio.2012.07.010
doi: 10.1016/j.ydbio.2012.07.010
pubmed: 22824426
Imarazene B, Beille S, Jouanno E et al (2021) Primordial germ cell migration and histological and molecular characterization of gonadal differentiation in Pachón Cavefish Astyanax mexicanus. Sex Dev 14:80–98. https://doi.org/10.1159/000513378
doi: 10.1159/000513378
Kurokawa H, Saito D, Nakamura S et al (2007) Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci 104:16958–16963. https://doi.org/10.1073/pnas.0609932104
doi: 10.1073/pnas.0609932104
pubmed: 17940041
pmcid: 2040408
Lebrun C, Billard R, Jalabert B (1982) Changes in the number of germ cells in the gonads of the rainbow trout (Salmo gairdneri) during the first 10 post-hatching weeks. Reprod Nutr Dev 22:405–412. https://doi.org/10.1051/rnd:19820312
doi: 10.1051/rnd:19820312
pubmed: 7156490
Lewis ZR, McClellan MC, Postlethwait JH et al (2008) Female-specific increase in primordial germ cells marks sex differentiation in threespine stickleback (Gasterosteus aculeatus). J Morphol 269:909–921. https://doi.org/10.1002/jmor.10608
doi: 10.1002/jmor.10608
pubmed: 18157863
pmcid: 7220811
Liu W, Li S-Z, Li Z et al (2015) Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence. BMC Genomics 16:971. https://doi.org/10.1186/s12864-015-2130-z
doi: 10.1186/s12864-015-2130-z
pubmed: 26582363
pmcid: 4652418
Martins RS, Gomez A, Zanuy S, Carrillo M, Canario AV, (2015) Photoperiodic modulation of circadian clock and reproductive axis gene expression in the pre-pubertal European sea bass brain. PLoS One 10(12):e0144158
Nakamura S, Watakabe I, Nishimura T et al (2012) Hyperproliferation of mitotically active germ cells due to defective anti-Müllerian hormone signaling mediates sex reversal in medaka. Development 139:2283–2287. https://doi.org/10.1242/dev.076307
doi: 10.1242/dev.076307
pubmed: 22627284
Navarro-Martín L, Viñas J, Ribas L, Díaz N, Gutiérrez A, Di Croce L, Piferrer F (2011) DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet 7(12)
Nishimura T, Yamada K, Fujimori C et al (2018) Germ cells in the teleost fish medaka have an inherent feminizing effect. PLOS Genet 14:e1007259. https://doi.org/10.1371/journal.pgen.1007259
doi: 10.1371/journal.pgen.1007259
pubmed: 29596424
pmcid: 5875746
Olsen LC, Aasland R, Fjose A (1997) A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 66:95–105. https://doi.org/10.1016/S0925-4773(97)00099-3
doi: 10.1016/S0925-4773(97)00099-3
pubmed: 9376327
Ospina-Álvarez N, Piferrer F (2008) Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS ONE 3:e2837. https://doi.org/10.1371/journal.pone.0002837
doi: 10.1371/journal.pone.0002837
pubmed: 18665231
pmcid: 2481392
Piferrer F, Blázquez M, Navarro L, González A (2005) Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol 142:102–110. https://doi.org/10.1016/j.ygcen.2005.02.011
doi: 10.1016/j.ygcen.2005.02.011
pubmed: 15862554
Roblin C and Bruslé J (1983) Ontogenèse gonadique et différenciation sexuelle du Loup Dicentrarchus labrax, en conditions d'élevage. Reprod Nutr Dévelop, vol 23. pp 115–127. https://doi.org/10.1051/rnd:19830110
Sadoul B, Alfonso S, Bessa E, Bouchareb A, Blondeau-Bidet E, Clair P, Chatain B, Begout ML, Geffroy B (2018) Enhanced brain expression of genes related to cell proliferation and neural differentiation is associated with cortisol receptor expression in fishes. General and Comparative Endocrinology 267:76–81
Sakae Y, Oikawa A, Sugiura Y, et al (2020) Starvation causes female-to-male sex reversal through lipid metabolism in the teleost fish, medaka (Olyzias latipes). Biol Open 9 https://doi.org/10.1242/bio.050054
Shinomiya A, Tanaka M, Kobayashi T et al (2000) The vasa-like gene, olvas, identifies the migration path of primordial germ cells during embryonic body formation stage in the medaka, Oryzias latipes. Dev Growth Differ 42:317–326. https://doi.org/10.1046/j.1440-169x.2000.00521.x
doi: 10.1046/j.1440-169x.2000.00521.x
pubmed: 10969731
Slanchev K, Stebler J, de la Cueva-Méndez G, Raz E (2005) Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc Natl Acad Sci U S A 102:4074–4079. https://doi.org/10.1073/pnas.0407475102
doi: 10.1073/pnas.0407475102
pubmed: 15728735
pmcid: 549510
Stavrakidis-Zachou O, Papandroulakis N, Lika K (2019)A DEB model for European sea bass (Dicentrarchus labrax): Parameterisation and application in aquaculture. Journal of Sea Research vol 143, pp 262–271
Strome S, Updike D (2015) Specifying and protecting germ cell fate. Nat Rev Mol Cell Biol 16:406–416. https://doi.org/10.1038/nrm4009
doi: 10.1038/nrm4009
pubmed: 26122616
pmcid: 4698964
Tao B, Liao X, Chen L et al (2022) Germ cells are not essential for sexual dimorphism of gonads in common carp. C Carpio l Aquaculture 547:737501. https://doi.org/10.1016/j.aquaculture.2021.737501
doi: 10.1016/j.aquaculture.2021.737501
Tovar-Bohórquez O, McKenzie D, Crestel D et al (2024) Thermal modulation of energy allocation during sex determination in the European sea bass (Dicentrarchus labrax). Gene 927:148721. https://doi.org/10.1016/j.gene.2024.148721
doi: 10.1016/j.gene.2024.148721
pubmed: 38925525
Tzung K-W, Goto R, Saju JM et al (2015) Early depletion of primordial germ cells in zebrafish promotes testis formation. Stem Cell Rep 4:61–73. https://doi.org/10.1016/j.stemcr.2014.10.011
doi: 10.1016/j.stemcr.2014.10.011
Vandeputte M, Dupont-Nivet M, Chavanne H, Chatain B (2007) A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics 176:1049–1057. https://doi.org/10.1534/genetics.107.072140
doi: 10.1534/genetics.107.072140
pubmed: 17435246
pmcid: 1894574
Vandeputte M, Clota F, Sadoul B et al (2020) Low temperature has opposite effects on sex determination in a marine fish at the larval/postlarval and juvenile stages. Ecol Evol 10:13825–13835. https://doi.org/10.1002/ece3.6972
doi: 10.1002/ece3.6972
pubmed: 33391683
pmcid: 7771145
Wargelius A, Leininger S, Skaftnesmo KO et al (2016) Dnd knockout ablates germ cells and demonstrates germ cell independent sex differentiation in Atlantic salmon. Sci Rep 6:21284. https://doi.org/10.1038/srep21284
doi: 10.1038/srep21284
pubmed: 26888627
pmcid: 4758030
Ye D, Zhu L, Zhang Q et al (2019) Abundance of early embryonic primordial germ cells promotes zebrafish female differentiation as revealed by lifetime labeling of germline. Mar Biotechnol 21:217–228. https://doi.org/10.1007/s10126-019-09874-1
doi: 10.1007/s10126-019-09874-1
Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124:3157–3165. https://doi.org/10.1242/dev.124.16.3157
doi: 10.1242/dev.124.16.3157
pubmed: 9272956
Yu Y, Chen M, Lu Z, et al (2022) High-temperature stress will put the thermo-sensitive teleost yellow catfish (Tachysurus fulvidraco) in danger through reducing reproductivity. Ecotoxicol Environ Saf 239 https://doi.org/10.1016/j.ecoenv.2022.113638