TY - JOUR
T1 - Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
AU - Burguera, Demian
AU - Marquez, Yamile
AU - Racioppi, Claudia
AU - Permanyer, Jon
AU - Torres-Méndez, Antonio
AU - Esposito, Rosaria
AU - Albuixech-Crespo, Beatriz
AU - Fanlo, Lucía
AU - D'Agostino, Ylenia
AU - Gohr, Andre
AU - Navas-Perez, Enrique
AU - Riesgo, Ana
AU - Cuomo, Claudia
AU - Benvenuto, Giovanna
AU - Christiaen, Lionel A.
AU - Martí, Elisa
AU - D'Aniello, Salvatore
AU - Spagnuolo, Antonietta
AU - Ristoratore, Filomena
AU - Arnone, Maria Ina
AU - Garcia-Fernàndez, Jordi
AU - Irimia, Manuel
N1 - Funding Information:
We thank Eduard Llorente for drawing the metazoan illustrations, Carlos Herrera and Jacobo Cela for helping with the experiments, Daniel Richter for providing access to unpublished choanoflagellate resources, and Hector Escrivà and Stephanie Bertrand for providing access to amphioxus animals. We also thank Jose Luis Gomez-Skarmeta, Ignacio Maeso and James Sharpe for critical reading of the manuscript and helpful suggestions. Animal silhouettes from Fig. 5, Supplementary Figs. 7–9 were obtained from PhyloPic. RNA sequencing was performed at the CRG Genomics facility, and histological sections were done with the help of the Histology Unit. This work has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No ERC-StG-LS2-637591 to M.I.), the Spanish Ministry of Economy and Competitiveness (grant BFU2014-58908P to J.G.-F, BFU2014-55076-P to M.I., and the ‘Centro de Excelencia Severo Ochoa 2013–2017’, SEV-2012-0208), and ICREA - Generalitat de Catalunya (Academia Prize to J.G.-F). We acknowledge the support of the CERCA Programme/Generalitat de Cata-lunya. D.B. held an APIF fellowship from University of Barcelona, Y.M. an EMBO Long Term postdoctoral fellowship (ALTF 1505-2015), C.R. an EMBO long-term fellowship (ALTF 1608-2014), ATM an FPI-SO fellowship.
Publisher Copyright:
© 2017 The Author(s).
PY - 2017/12/1
Y1 - 2017/12/1
N2 - Epithelial-mesenchymal interactions are crucial for the development of numerous animal structures. Thus, unraveling how molecular tools are recruited in different lineages to control interplays between these tissues is key to understanding morphogenetic evolution. Here, we study Esrp genes, which regulate extensive splicing programs and are essential for mammalian organogenesis. We find that Esrp homologs have been independently recruited for the development of multiple structures across deuterostomes. Although Esrp is involved in a wide variety of ontogenetic processes, our results suggest ancient roles in non-neural ectoderm and regulating specific mesenchymal-To-epithelial transitions in deuterostome ancestors. However, consistent with the extensive rewiring of Esrp-dependent splicing programs between phyla, most developmental defects observed in vertebrate mutants are related to other types of morphogenetic processes. This is likely connected to the origin of an event in Fgfr, which was recruited as an Esrp target in stem chordates and subsequently co-opted into the development of many novel traits in vertebrates.
AB - Epithelial-mesenchymal interactions are crucial for the development of numerous animal structures. Thus, unraveling how molecular tools are recruited in different lineages to control interplays between these tissues is key to understanding morphogenetic evolution. Here, we study Esrp genes, which regulate extensive splicing programs and are essential for mammalian organogenesis. We find that Esrp homologs have been independently recruited for the development of multiple structures across deuterostomes. Although Esrp is involved in a wide variety of ontogenetic processes, our results suggest ancient roles in non-neural ectoderm and regulating specific mesenchymal-To-epithelial transitions in deuterostome ancestors. However, consistent with the extensive rewiring of Esrp-dependent splicing programs between phyla, most developmental defects observed in vertebrate mutants are related to other types of morphogenetic processes. This is likely connected to the origin of an event in Fgfr, which was recruited as an Esrp target in stem chordates and subsequently co-opted into the development of many novel traits in vertebrates.
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U2 - 10.1038/s41467-017-01961-y
DO - 10.1038/s41467-017-01961-y
M3 - Article
C2 - 29180615
AN - SCOPUS:85035791355
VL - 8
JO - Nature Communications
JF - Nature Communications
SN - 2041-1723
IS - 1
M1 - 1799
ER -