foxn4 Expression Pattern Suggests Its Association with Neurosensory Cells in the White Sea Hydrozoan Sarsia loveni

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Abstract

The foxn4 is one of the key transcription factor genes controlling retinal formation in vertebrates. However, it is not clear whether its association with light-sensitive organ formation is evolutionary conserved. To answer this question, we tested whether the expression of this gene is localized within light-sensitive organs in a representative of basal Metazoa, the hydroid Sarsia lovenii (Hydrozoa, Cnidaria). Usually, the life cycle of hydroids includes stages of a pelagic medusa and a benthic polyp. However, in many species, attached medusoids, in which many medusa structures are reduced, form instead of free-swimming medusa. The White Sea hydrozoan Sarsia lovenii is an exceptional example of the species, in which polyps of different haplotypes produce either pelagic medusae or attached medusoids. Comparison of gene expression in medusae and medusoids of S. lovenii is a promising model to study how the formation of morphological traits is regulated in hydrozoan cnidarians. We compared the spatial pattern of Foxn4 expression in medusae and medusoids of S. lovenii by in situ hybridization. In medusae, Foxn4 is expressed not in the photoreceptive ocelli, but in the ectoderm of the tentacle bulb around the ocellus. Although, unlike medusae, S. lovenii medusoids lack ocelli, we detected Foxn4 expression in their reduced tentacle bulbs. It is known that the tentacle bulb in hydrozoan medusae is a zone of localized formation of nematocytes, which are considered to be derivatives of mechanosensory cells. Thus, our results indicate that, in medusae and medusoids of S. lovenii, the foxn4 is not associated with the formation of photoreceptor organs, as in vertebrates. However, it may be associated with nematocytes, another type of neurosensory cells.

About the authors

A. A. Vetrova

Koltzov Institute of Developmental Biology of the Russian Academy of Sciences

Email: s.kremnyov@gmail.com
Russia, Moscow

A. A. Prudkovsky

Lomonosov Moscow State University

Email: s.kremnyov@gmail.com
Russia, Moscow

S. V. Kremnyov

Koltzov Institute of Developmental Biology of the Russian Academy of Sciences; Lomonosov Moscow State University

Author for correspondence.
Email: s.kremnyov@gmail.com
Russia, Moscow; Russia, Moscow

References

  1. Chevalier S., Martin A., Leclère L. et al. Polarised expression of FoxB and FoxQ2 genes during development of the hydrozoan Clytia hemisphaerica. // Dev. Genes. Evol. 2006. V. 216. № 11. P. 709–720. https://doi.org/10.1007/s00427-006-0103-6
  2. Condamine T., Jager M., Leclère L. et al. Molecular characterisation of a cellular conveyor belt in Clytia medusae // Dev. Biol. 2019. V.456. № 2. P. 212–225. https://doi.org/10.1016/j.ydbio.2019.09.001
  3. Denker E., Manuel M., Leclère L. et al. Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria) // Dev Biol. 2008. V. 315. № 1. P. 99–113. https://doi.org/10.1016/j.ydbio.2007.12.023
  4. Edwards C. The hydroids and medusae Sarsia occulta sp. nov., Sarsia tubulosa and Sarsia loveni // J. Mar. Biol. Assoc. 1978. V. 58. № 2. P. 291–311.
  5. Genikhovich G., Technau U. In situ hybridization of starlet sea anemone (Nematostella vectensis) embryos, larvae, and polyps // Cold Spring Harb Protoc. 2009. V. 2009. № 9. P. pdb. prot5282. https://doi.org/10.1101/pdb.prot5282
  6. Golson M.L., Kaestner K.H. Fox transcription factors: from development to disease. // Development. 2016. V. 143. № 24. P. 4558–4570. https://doi.org/10.1242/dev.112672
  7. Kozmik Z. Pax genes in eye development and evolution // Curr Opin Genet Dev. 2005. V. 15. № 4. P. 430–438. https://doi.org/10.1016/j.gde.2005.05.001
  8. Kozmik Z., Daube M., Frei E. et al. Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions // Dev cell. 2003. V. 5. № 5. P. 773–785. https://doi.org/10.1016/S1534-5807(03)00325-3
  9. Kupaeva D.M., Vetrova A.A., Kraus Y.A. et al. Epithelial folding in the morphogenesis of the colonial marine hydrozoan, Dynamena pumila // Biosystems. 2018. V. 173. P. 157–164.
  10. Leclère L., Horin C., Chevalier S. et al. The genome of the jellyfish Clytia hemisphaerica and the evolution of the cnidarian life-cycle // Nat. Ecol. Evol. 2019. V. 3. № 5. P. 801–810. https://doi.org/10.1038/s41559-019-0833-2
  11. Leclère L., Jager M., Barreau C. et al. Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia // Dev. Biol. 2012 V. 364. № 2. P. 236–248. https://doi.org/10.1016/j.ydbio.2012.01.018
  12. Liu S., Liu X., Li S. et al. Foxn4 is a temporal identity factor conferring mid/late-early retinal competence and invoed in retinal synaptogenesis // Proc. Natl. Acad. Sci. USA. 2020. V. 117. № 9. P. 5016–5027. https://doi.org/10.1073/pnas.1918628117
  13. Mochizuki K., Nishimiya-Fujisawa C., Fujisawa T. Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra // Dev. Genes. Evol. 2001. V. 211. № 6. P. 299–308. https://doi.org/10.1007/s004270100156
  14. Mochizuki K., Sano H., Kobayashi S. et al. Expression and evolutionary conservation of nanos-related genes in Hydra // Dev. Genes. Evol. 2000. V. 210. № 12. P. 591–602. https://doi.org/10.1007/s004270000105
  15. Oliver D., Brinkmann M., Sieger T. et al. Hydrozoan nematocytes send and receive synaptic signals induced by mechano-chemical stimuli // J. Exp. Biol. 2008. V. 211. № 17. P. 2876–2888. https://doi.org/10.1242/jeb.018515
  16. Prudkovsky A.A., Ekimova I.A., Neretina T.V. A case of nascent speciation: unique polymorphism of gonophores within hydrozoan Sarsia lovenii // Sci. Rep. 2019. V. 9. № 1. P. 1–13. https://doi.org/10.1038/s41598-019-52026-7
  17. Rebscher N., Volk C., Teo R. et al. The germ plasm component Vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata // Dev. Dyn. 2008. V. 237. № 6. P. 1736–1745. https://doi.org/10.1002/dvdy.21562
  18. Seipel K., Yanze N., Schmid V. The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea // Int. J. Dev. Biol. 2004. V. 48. № 1. P. 1–7. https://doi.org/10.1387/ijdb.15005568
  19. Singla C.L., Weber C. Fine structure of the ocellus of Sarsia tubulosa (Hydrozoa, Anthomedusae) // Zoomorphology. 1982. V. 100. № 1. P. 11–22. https://doi.org/10.1007/BF00312197
  20. Suga H., Tschopp P., Graziussi D.F. et al. Flexibly deployed Pax genes in eye development at the early evolution of animals demonstrated by studies on a hydrozoan jellyfish // Proc. Natl. Acad. Sci. USA. 2010. V. 107. № 32. P. 14263–14268.
  21. Vetrova A.A., Prudkovsky A.A., Kremnyov S.V. Distribution of nematocytes differs in two types of gonophores in hydrozoan Sarsia lovenii // bioRxiv 2023. P. 2023.03. https://doi.org/10.1101/2023.03.22.533798
  22. Wawersik S., Maas R.L. Vertebrate eye development as modeled in Drosophila // Hum Mol Genet. 2000. V. 9. № 6. P. 917–25. https://doi.org/10.1093/hmg/9.6.917

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Copyright (c) 2023 А.А. Ветрова, А.А. Прудковский, С.В. Кремнев