On the origin and evolutionary history of NANOG.
Though pluripotency is well characterized in mammals, many questions remain to be resolved regarding its evolutionary history. A necessary prerequisite for addressing this issue is to determine the phylogenetic distributions and orthology relationships of the transcription factor families sustaining or modulating this property. In mammals, the NANOG homeodomain transcription factor is one of the core players in the pluripotency network. However, its evolutionary history has not been thoroughly studied, hindering the interpretation of comparative studies. To date, the NANOG family was thought to be monogenic, with numerous pseudogenes described in mammals, including a tandem duplicate in Hominidae. By examining a wide-array of craniate genomes, we provide evidence that the NANOG family arose at the latest in the most recent common ancestor of osteichthyans and that NANOG genes are frequently found as tandem duplicates in sarcopterygians and as a single gene in actinopterygians. Their phylogenetic distribution is thus reminiscent of that recently shown for Class V POU paralogues, another key family of pluripotency-controlling factors. However, while a single ancestral duplication has been reported for the Class V POU family, we suggest that multiple independent duplication events took place during evolution of the NANOG family. These multiple duplications could have contributed to create a layer of complexity in the control of cell competence and pluripotency, which could explain the discrepancies relative to the functional evolution of this important gene family. Further, our analysis does not support the hypothesis that loss of NANOG and emergence of the preformation mode of primordial germ cell specification are causally linked. Our study therefore argues for the need of further functional comparisons between NANOG paralogues, notably regarding the novel duplicates identified in sauropsids and non-eutherian mammals.
Département Régulations, Développement et Diversité Moléculaire, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Paris, France ; Institut de Biologie du Développement de Marseille, Aix-Marseille Université, Centre National de la Recherche Scientifique, Marseille, France.
Pierluigi
P
Scerbo
Département Régulations, Développement et Diversité Moléculaire, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Paris, France ; Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Ecole Normale Supérieure de Lyon, Centre National de la Recherche Scientifique, Lyon, France ; Department for Evolutionary Biology, Max-Planck-Institute for Developmental Biology, Tuebingen, Germany.
Gabriel V
GV
Markov
Département Régulations, Développement et Diversité Moléculaire, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Paris, France ; WatchFrog S.A., Evry, France.
Céline
C
Vivien
Institut de Biologie du Développement de Marseille, Aix-Marseille Université, Centre National de la Recherche Scientifique, Marseille, France.
Laurent
L
Kodjabachian
Département Régulations, Développement et Diversité Moléculaire, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Paris, France.
Barbara
B
Demeneix
Département Régulations, Développement et Diversité Moléculaire, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Paris, France.
Laurent
L
Coen
Département Régulations, Développement et Diversité Moléculaire, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Paris, France.
Fabrice
F
Girardot
D000818:Animals; D019143:Evolution, Molecular; D056426:Genetic Loci; D018398:Homeodomain Proteins / Q000235:genetics*; D006801:Humans; D000071317:Nanog Homeobox Protein; D010802:Phylogeny; D017386:Sequence Homology, Amino Acid; D026801:Synteny / Q000235:genetics
D018398:Homeodomain Proteins; C486780:NANOG protein, human; D000071317:Nanog Homeobox Protein