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

Annona, Giovanni and Sato, Iori and Pascual-Anaya, Juan and Osca, David and Braasch, Ingo and Voss, Randal and Stundl, Jan and Soukup, Vladimir and Ferrara, Allyse and Fontenot, Quenton and Kuratani, Shigeru and Postlethwait, John H. and D’Aniello, Salvatore (2022) Evolution of the nitric oxide synthase family in vertebrates and novel insights in gill development. Proceedings of the Royal Society B: Biological Sciences, 289 (1980). Art. No. 20220667. ISSN 0962-8452. PMCID PMC9363997. doi:10.1098/rspb.2022.0667. https://resolver.caltech.edu/CaltechAUTHORS:20210621-171714685

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1098/rspb.2022.0667DOIArticle
https://doi.org/10.1101/2021.06.14.448362DOIDiscussion Paper
ORCID:
AuthorORCID
Annona, Giovanni0000-0001-7806-6761
Sato, Iori0000-0001-7077-6646
Pascual-Anaya, Juan0000-0003-3429-9453
Osca, David0000-0001-5259-9420
Braasch, Ingo0000-0003-4766-611X
Stundl, Jan0000-0002-3740-3378
Soukup, Vladimir0000-0002-1914-283X
Kuratani, Shigeru0000-0001-9717-7221
Postlethwait, John H.0000-0002-5476-2137
D’Aniello, Salvatore0000-0001-7294-1465
Additional Information:© 2022 The Author(s). Published by the Royal Society. Manuscript received 02/06/2022; Manuscript accepted 19/07/2022; Published online 10/08/2022; Published in print 10/08/2022. 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. 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. Data accessibility: Accession numbers of protein sequences used in the phylogenetic analysis are available in the electronic supplementary material, table S1. Primer sequences used for the synthesis of in situ hybridization riboprobes and in qRT-PCR experiments are given in the electronic supplementary material, table S3. Electronic supplementary material is available online [58]. Authors' contributions: G.A.: conceptualization, data curation, formal analysis, investigation, methodology, writing—original draft, writing—review and editing; I.S.: investigation, methodology; J.P.-A.: conceptualization, data curation, formal analysis, investigation, methodology, validation, writing—original draft, writing—review and editing; D.O.: data curation, formal analysis, writing—review and editing; I.B.: writing—review and editing; R.V.: data curation, investigation, writing—review and editing; J.S.: data curation, investigation, writing—review and editing; V.S.: conceptualization, data curation, investigation, methodology, writing—review and editing; A.F.: data curation, formal analysis, investigation, writing—review and editing; Q.F.: data curation, formal analysis, investigation, writing—review and editing; S.K.: supervision; J.H.P.: conceptualization, data curation, investigation, methodology, supervision, writing—review and editing; S.D.: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, supervision, validation, writing—original draft, writing—review and editing. All authors gave final approval for publication and agreed to be held accountable for the work performed therein. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Programma Operativo Regionale CampaniaFSE 2014/2020
European Molecular Biology Organization (EMBO)6936
Marie Curie Fellowship897949
Charles University204069
Charles UniversitySVV260571/2020
NIHP40OD019794
NIHR01 OD011116
NSFIOS-2029216
Stazione Zoologica Anton Dohrn NapoliUNSPECIFIED
Subject Keywords:vertebrate evolution, genome duplication, gene duplication and loss, nos, phylogenomics, synteny
Issue or Number:1980
PubMed Central ID:PMC9363997
DOI:10.1098/rspb.2022.0667
Record Number:CaltechAUTHORS:20210621-171714685
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210621-171714685
Official Citation:Annona G et al. 2022 Evolution of the nitric oxide synthase family in vertebrates and novel insights in gill development. Proc. R. Soc. B 289: 20220667. https://doi.org/10.1098/rspb.2022.0667
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109507
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:21 Jun 2021 17:34
Last Modified:17 Aug 2022 17:47

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