Lineage-specific duplication of amphioxus retinoic acid degrading enzymes (CYP26) resulted in sub-functionalization of patterning and homeostatic roles

BMC Evolutionary Biology

Research Article

Susana Alvarez¹  Angel R. De Lera¹  Pascale Chevret²  Maria Theodosiou³  Jie Chen⁴  Vincent Laudet⁵  Michael Schubert⁶  João E. Carvalho⁶  Jenifer C. Croce⁶ 

[1] Departamento de Química Organica, Facultad de Química, Universidade de Vigo, 36310, Vigo, Spain;Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, 43 Boulevard du 11 novembre 1918, 69622, Villeurbanne, France;Molecular Zoology Team, Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Lyon 1, CNRS, INRA, Ecole Normale Supérieure de Lyon, 46 Allée d’Italie, 69364, Lyon, Cedex 07, France;Molecular Zoology Team, Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Lyon 1, CNRS, INRA, Ecole Normale Supérieure de Lyon, 46 Allée d’Italie, 69364, Lyon, Cedex 07, France;Present Address: Key Laboratory of Freshwater Aquatic Genetic Resources, Shanghai Ocean University, Huchenghuan Road 999, 201306, Shanghai, China;Molecular Zoology Team, Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Lyon 1, CNRS, INRA, Ecole Normale Supérieure de Lyon, 46 Allée d’Italie, 69364, Lyon, Cedex 07, France;Present Address: Observatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232, Université Pierre et Marie Curie Paris, 1 avenue du Fontaulé, 66650, Banyuls-sur-Mer, France;Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-Mer, Observatoire Océanologique de Villefranche-sur-Mer, 181 Chemin du Lazaret, 06230, Villefranche-sur-Mer, France;

关键词: Branchiostoma lanceolatum;    Cephalochordate;    Duplication-Degeneration-Complementation (DDC) model;    Lancelet;    Retinoic acid (RA) signaling;   

DOI  :  10.1186/s12862-016-0863-1

 received in 2016-07-06, accepted in 2016-12-21,  发布年份 2017

来源: Springer

【 摘 要 】

BackgroundDuring embryogenesis, tight regulation of retinoic acid (RA) availability is fundamental for normal development. In parallel to RA synthesis, a negative feedback loop controlled by RA catabolizing enzymes of the cytochrome P450 subfamily 26 (CYP26) is crucial. In vertebrates, the functions of the three CYP26 enzymes (CYP26A1, CYP26B1, and CYP26C1) have been well characterized. By contrast, outside vertebrates, little is known about CYP26 complements and their biological roles. In an effort to characterize the evolutionary diversification of RA catabolism, we studied the CYP26 genes of the cephalochordate amphioxus (Branchiostoma lanceolatum), a basal chordate with a vertebrate-like genome that has not undergone the massive, large-scale duplications of vertebrates.ResultsIn the present study, we found that amphioxus also possess three CYP26 genes (CYP26-1, CYP26-2, and CYP26-3) that are clustered in the genome and originated by lineage-specific duplication. The amphioxus CYP26 cluster thus represents a useful model to assess adaptive evolutionary changes of the RA signaling system following gene duplication. The characterization of amphioxus CYP26 expression, function, and regulation by RA signaling demonstrated that, despite the independent origins of CYP26 duplicates in amphioxus and vertebrates, they convergently assume two main roles during development: RA-dependent patterning and protection against fluctuations of RA levels. Our analysis suggested that in amphioxus RA-dependent patterning is sustained by CYP26-2, while RA homeostasis is mediated by CYP26-1 and CYP26-3. Furthermore, comparisons of the regulatory regions of CYP26 genes of different bilaterian animals indicated that a CYP26-driven negative feedback system was present in the last common ancestor of deuterostomes, but not in that of bilaterians.ConclusionsAltogether, this work reveals the evolutionary origins of the RA-dependent regulation of CYP26 genes and highlights convergent functions for CYP26 enzymes that originated by independent duplication events, hence establishing a novel selective mechanism for the genomic retention of gene duplicates.

【 授权许可】

CC BY   
© The Author(s). 2017