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Evolution of the nitric oxide synthase family in vertebrates and novel insights in gill development

  • Giovanni Annona
  • , Iori Sato
  • , Juan Pascual-Anaya
  • , David Osca
  • , Ingo Braasch
  • , Randal Voss
  • , Jan Stundl
  • , Vladimir Soukup
  • , Allyse Ferrara
  • , Quenton Fontenot
  • , Shigeru Kuratani
  • , John H. Postlethwait
  • , Salvatore D'Aniello

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Nitric oxide (NO) is an ancestral key signalling molecule essential for life and has enormous versatility in biological systems, including cardiovascular homeostasis, neurotransmission and immunity. Although our knowledge of NO synthases (Nos), the enzymes that synthesize NO in vivo, is substantial, the origin of a large and diversified repertoire of nos gene orthologues in fishes with respect to tetrapods remains a puzzle. The recent identification of nos3 in the ray-finned fish spotted gar, which was considered lost in this lineage, changed this perspective. This finding prompted us to explore nos gene evolution, surveying vertebrate species representing key evolutionary nodes. This study provides noteworthy findings: first, nos2 experienced several lineage-specific gene duplications and losses. Second, nos3 was found to be lost independently in two different teleost lineages, Elopomorpha and Clupeocephala. Third, the expression of at least one nos paralogue in the gills of developing shark, bichir, sturgeon, and gar, but not in lamprey, suggests that nos expression in this organ may have arisen in the last common ancestor of gnathostomes. These results provide a framework for continuing research on nos genes' roles, highlighting subfunctionalization and reciprocal loss of function that occurred in different lineages during vertebrate genome duplications.

Original languageEnglish
Article number20220667
JournalProceedings of the Royal Society B: Biological Sciences
Volume289
Issue number1980
DOIs
StatePublished - Aug 10 2022

Bibliographical note

Publisher Copyright:
© 2022 The Author(s).

Funding

G.A. was supported by the Research grant POR Campania FSE 2014/2020 (IT) and by the EMBO Short Term Fellowship (no. 6936) to visit the Postlethwait laboratory in Oregon (USA) and for the field trip in Louisiana (USA). J.S. is supported by a Marie Skłodowska-Curie grant agreement no. 897949. V.S. is supported by the Charles University Research Centre program no. 204069 and grant no. SVV260571/2020. R.V. and the Ambystoma Genetic Stock Center are supported by US NIH (P40OD019794). J.H.P. and I.B. are supported by the R01 OD011116 grant from the US NIH. I.B. is supported by the US NSF EDGE grant no. 2029216. S.D. is supported by the NOEVO grant from the SZN. Acknowledgements G.A. was supported by the Research grant POR Campania FSE 2014/2020 (IT) and by the EMBO Short Term Fellowship (no. 6936) to visit the Postlethwait laboratory in Oregon (USA) and for the field trip in Louisiana (USA). J.S. is supported by a Marie SkÅ odowska-Curie grant agreement no. 897949. V.S. is supported by the Charles University Research Centre program no. 204069 and grant no. SVV260571/2020. R.V. and the Ambystoma Genetic Stock Center are supported by US NIH (P40OD019794). J.H.P. and I.B. are supported by the R01 OD011116 grant from the US NIH. I.B. is supported by the US NSF EDGE We thank Fumiaki Sugahara for the interpretation of arctic lamprey results, Anna Pospisilova for technical assistance with bichir and sturgeon in situ hybridizations, and Martin Psenicka, Roman Franek, Michaela Fucikova, Marek Rodina, David Gela, Martin Kahanec for sterlet sturgeon spawns. A special thanks to Robert Cerny for the establishment of the African bichir colony at the Charles University in Prague. The sturgeon work was supported by the Ministry of Education, Youth and Sports of the Czech Republic, project Cenakva (LM2018099) and project Biodiversity (CZ.02.1.01/0.0/0.0/16_025/007370). We also thank Jordi Paps and Giacinto De Vivo for their help on phylogenetic inferences, and to Silvia Perea and Iker Irisarri for their help in the selection analyses.

FundersFunder number
Stazione Zoologica Anton Dohrn Napoli
National Institutes of Health (NIH)
Horizon 2020 Framework Programme
US NIHR01 OD011116, P40OD019794
H2020 Marie Skłodowska-Curie Actions897949
Univerzita Karlova v PrazeSVV260571/2020, 204069
National Science Foundation Arctic Social Science Program2029216
Ministerstvo Školství, Mládeže a TělovýchovyLM2018099, CZ.02.1.01/0.0/0.0/16_025/007370
NIH Office of the DirectorR01OD011116, P40OD019794
European Molecular Biology Organization6936

    Keywords

    • Gene duplication and loss
    • Genome duplication
    • Nos
    • Phylogenomics
    • Synteny
    • Vertebrate evolution

    ASJC Scopus subject areas

    • General Immunology and Microbiology
    • General Biochemistry, Genetics and Molecular Biology
    • General Environmental Science
    • General Agricultural and Biological Sciences

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