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; Manuel Irimia

doi:10.1038/s41467-017-01961-y

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 ArnoneJordi Garcia-Fernàndez, Manuel Irimia

Biology and Genomics

Research output: Contribution to journal › Article › peer-review

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.

Original language	English (US)
Article number	1799
Journal	Nature communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-01961-y
State	Published - Dec 1 2017

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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10.1038/s41467-017-01961-y

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Burguera, D., Marquez, Y., Racioppi, C., Permanyer, J., Torres-Méndez, A., Esposito, R., Albuixech-Crespo, B., Fanlo, L., D'Agostino, Y., Gohr, A., Navas-Perez, E., Riesgo, A., Cuomo, C., Benvenuto, G., Christiaen, L. A., Martí, E., D'Aniello, S., Spagnuolo, A., Ristoratore, F., ... Irimia, M. (2017). Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes. Nature communications, 8(1), [1799]. https://doi.org/10.1038/s41467-017-01961-y

Burguera, D, Marquez, Y, Racioppi, C, Permanyer, J, Torres-Méndez, A, Esposito, R, Albuixech-Crespo, B, Fanlo, L, D'Agostino, Y, Gohr, A, Navas-Perez, E, Riesgo, A, Cuomo, C, Benvenuto, G, Christiaen, LA, Martí, E, D'Aniello, S, Spagnuolo, A, Ristoratore, F, Arnone, MI, Garcia-Fernàndez, J & Irimia, M 2017, 'Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes', Nature communications, vol. 8, no. 1, 1799. https://doi.org/10.1038/s41467-017-01961-y

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title = "Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes",

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.",

author = "Demian Burguera and Yamile Marquez and Claudia Racioppi and Jon Permanyer and Antonio Torres-M{\'e}ndez and Rosaria Esposito and Beatriz Albuixech-Crespo and Luc{\'i}a Fanlo and Ylenia D'Agostino and Andre Gohr and Enrique Navas-Perez and Ana Riesgo and Claudia Cuomo and Giovanna Benvenuto and Christiaen, {Lionel A.} and Elisa Mart{\'i} and Salvatore D'Aniello and Antonietta Spagnuolo and Filomena Ristoratore and Arnone, {Maria Ina} and Jordi Garcia-Fern{\`a}ndez and Manuel Irimia",

note = "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 Escriv{\`a} 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{\textquoteright}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 {\textquoteleft}Centro de Excelencia Severo Ochoa 2013–2017{\textquoteright}, 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: {\textcopyright} 2017 The Author(s).",

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doi = "10.1038/s41467-017-01961-y",

language = "English (US)",

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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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JF - Nature Communications

SN - 2041-1723

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

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