A novel evolutionary conserved mechanism of RNA stability regulates synexpression of primordial germ cell-specific genes prior to the sex-determination stage in medaka

Amaury Herpin (1, 2) , Cornelia Schmidt (2) , Susanne Kneitz (2) , Clara Gobe (3) , Martina Regensburger (2) , Aurélie Le Cam (1) , Jérôme Montfort (1) , Mateus C. Adolfi (2) , Christina Lillesaar (2) , Dagmar Wilhelm (4) , Michael Kraeussling (2) , Brigitte Mourot (1) , Béatrice Porcon (1) , Maëlle Pannetier (3) , Eric Pailhoux (3) , Laurence Ettwiller (5, 6) , Dirk Dolle (5, 6) , Yann Guiguen (1) , Manfred Schartl (2, 7, 8)

1 LPGP - Laboratoire de Physiologie et Génomique des Poissons
2 Physiological Chemistry, Biocenter
3 BDR - Biologie du Développement et Reproduction
4 Department of Anatomy & Neuroscience [Melbourne]
5 Department of Developmental Biology
6 Universität Heidelberg [Heidelberg] = Heidelberg University
7 Comprehensive Cancer Center Mainfranken
8 Hagler Institute for Advanced Study and Department of Biology

Dmrt1 is a highly conserved transcription factor, which is critically involved in regulation of gonad development of vertebrates. In medaka, a duplicate of dmrt1—acting as master sexdetermining gene—has a tightly timely and spatially controlled gonadal expression pattern. In addition to transcriptional regulation, a sequence motif in the 30 UTR (D3U-box) mediates transcript stability of dmrt1 mRNAs from medaka and other vertebrates. We show here that in medaka, two RNA-binding proteins with antagonizing properties target this D3U-box, promoting either RNA stabilization in germ cells or degradation in the soma. The D3U-box is also conserved in other germ-cell transcripts, making them responsive to the same RNA binding proteins. The evolutionary conservation of the D3U-box motif within dmrt1 genes of metazoans—together with preserved expression patterns of the targeting RNA binding proteins in subsets of germ cells—suggest that this new mechanism for controlling RNA stability is not restricted to fishes but might also apply to other vertebrates.

Mots clés: fish; germ-line cells; gonad; transcription factors; sex determination

Mots clés: poisson; adrianichthyidae; medaka; gonade; oryzias latipes; cellule germinale; reproduction; analyse de génome; histologie; détermination du sexe; protéine liaison rna; gène déterminant majeur du sexe; facteur de transcription; gène dmrt1; embryogénèse; expression des gènes; régulation de la transcription

Domaines: Sciences du Vivant [q-bio]

Amaury Herpin, Cornelia Schmidt, Susanne Kneitz, Clara Gobe, Martina Regensburger, et al.. A novel evolutionary conserved mechanism of RNA stability regulates synexpression of primordial germ cell-specific genes prior to the sex-determination stage in medaka. PLoS Biology, 2019, 17 (4), pp.1-29. ⟨10.1371/journal.pbio.3000185⟩. ⟨hal-02093379⟩