Welcome to the new version of CaltechAUTHORS. Login is currently restricted to library staff. If you notice any issues, please email coda@library.caltech.edu
Published August 10, 2022 | Supplemental Material + Accepted Version + Submitted
Journal Article Open

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

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.

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.

Attached Files

Accepted Version - eg2-pdf-AUTHOR-RS202207262110060451-RSPB20220667-2.pdf

Submitted - 2021.06.14.448362v1.full.pdf

Supplemental Material - 20449321.zip

Files

eg2-pdf-AUTHOR-RS202207262110060451-RSPB20220667-2.pdf
Files (10.8 MB)
Name Size Download all
md5:f9ca0525c906d72c011e26c1c085bb3d
10.0 MB Preview Download
md5:edc7c4dfd25705e0293836da84566371
20.1 kB Preview Download
md5:a3d1d4e860d2ab4e38aca83e9a80bf2a
758.2 kB Preview Download

Additional details

Created:
August 20, 2023
Modified:
December 21, 2023