Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes

Demian Burguera, Yamile Marquez, Claudia Racioppi, Jon Permanyer, Antonio Torres-Méndez, Rosaria Esposito, Beatriz Albuixech-Crespo, Lucía Fanlo, Ylenia D’Agostino, Andre Gohr, Enrique Navas-Perez, Ana Riesgo, Claudia Cuomo, Giovanna Benvenuto, Lionel A. Christiaen, Elisa Martí, Salvatore D’Aniello, Antonietta Spagnuolo, Filomena Ristoratore, Maria Ina Arnone (), Jordi Garcia-Fernàndez () and Manuel Irimia ()
Additional contact information
Demian Burguera: Barcelona Institute of Science and Technology (BIST)
Yamile Marquez: Barcelona Institute of Science and Technology (BIST)
Claudia Racioppi: Stazione Zoologica Anton Dohrn, Villa Comunale
Jon Permanyer: Barcelona Institute of Science and Technology (BIST)
Antonio Torres-Méndez: Barcelona Institute of Science and Technology (BIST)
Rosaria Esposito: Stazione Zoologica Anton Dohrn, Villa Comunale
Beatriz Albuixech-Crespo: School of Biology, and Institut de Biomedicina (IBUB), University of Barcelona
Lucía Fanlo: CSIC, Parc Científic de Barcelona
Ylenia D’Agostino: Stazione Zoologica Anton Dohrn, Villa Comunale
Andre Gohr: Barcelona Institute of Science and Technology (BIST)
Enrique Navas-Perez: School of Biology, and Institut de Biomedicina (IBUB), University of Barcelona
Ana Riesgo: Natural History Museum of London
Claudia Cuomo: Stazione Zoologica Anton Dohrn, Villa Comunale
Giovanna Benvenuto: Stazione Zoologica Anton Dohrn, Villa Comunale
Lionel A. Christiaen: Department of Biology, New York University
Elisa Martí: CSIC, Parc Científic de Barcelona
Salvatore D’Aniello: Stazione Zoologica Anton Dohrn, Villa Comunale
Antonietta Spagnuolo: Stazione Zoologica Anton Dohrn, Villa Comunale
Filomena Ristoratore: Stazione Zoologica Anton Dohrn, Villa Comunale
Maria Ina Arnone: Stazione Zoologica Anton Dohrn, Villa Comunale
Jordi Garcia-Fernàndez: School of Biology, and Institut de Biomedicina (IBUB), University of Barcelona
Manuel Irimia: Barcelona Institute of Science and Technology (BIST)

Nature Communications, 2017, vol. 8, issue 1, 1-15

Abstract: Abstract 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.

Date: 2017
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DOI: 10.1038/s41467-017-01961-y

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