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 Christiaen, Elisa Martí, Salvatore D'Aniello, Antonietta Spagnuolo, Filomena Ristoratore, Maria Ina ArnoneJordi Garcia-Fernàndez, Manuel Irimia

Research output: Contribution to journalArticle

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 languageEnglish (US)
Article number1799
JournalNature Communications
Volume8
Issue number1
DOIs
StatePublished - Dec 1 2017

Fingerprint

splicing
Vertebrates
vertebrates
Animals
Genes
Tissue
Chordata
Animal Structures
Defects
Ectoderm
Epithelial-Mesenchymal Transition
Organogenesis
stems
genes
animals
defects
interactions

ASJC Scopus subject areas

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

Cite this

Burguera, D., Marquez, Y., Racioppi, C., Permanyer, J., Torres-Méndez, A., Esposito, R., ... 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

Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes. / Burguera, Demian; Marquez, Yamile; Racioppi, Claudia; Permanyer, Jon; Torres-Méndez, Antonio; Esposito, Rosaria; Albuixech-Crespo, Beatriz; Fanlo, Lucía; D'Agostino, Ylenia; Gohr, Andre; Navas-Perez, Enrique; Riesgo, Ana; Cuomo, Claudia; Benvenuto, Giovanna; Christiaen, Lionel; Martí, Elisa; D'Aniello, Salvatore; Spagnuolo, Antonietta; Ristoratore, Filomena; Arnone, Maria Ina; Garcia-Fernàndez, Jordi; Irimia, Manuel.

In: Nature Communications, Vol. 8, No. 1, 1799, 01.12.2017.

Research output: Contribution to journalArticle

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, 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
Burguera, Demian ; Marquez, Yamile ; Racioppi, Claudia ; Permanyer, Jon ; Torres-Méndez, Antonio ; Esposito, Rosaria ; Albuixech-Crespo, Beatriz ; Fanlo, Lucía ; D'Agostino, Ylenia ; Gohr, Andre ; Navas-Perez, Enrique ; Riesgo, Ana ; Cuomo, Claudia ; Benvenuto, Giovanna ; Christiaen, Lionel ; Martí, Elisa ; D'Aniello, Salvatore ; Spagnuolo, Antonietta ; Ristoratore, Filomena ; Arnone, Maria Ina ; Garcia-Fernàndez, Jordi ; Irimia, Manuel. / Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes. In: Nature Communications. 2017 ; Vol. 8, No. 1.
@article{e2f0c467981c4116847bbf096a15c8e3,
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 Lionel Christiaen 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",
year = "2017",
month = "12",
day = "1",
doi = "10.1038/s41467-017-01961-y",
language = "English (US)",
volume = "8",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",
number = "1",

}

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

AU - Martí, Elisa

AU - D'Aniello, Salvatore

AU - Spagnuolo, Antonietta

AU - Ristoratore, Filomena

AU - Arnone, Maria Ina

AU - Garcia-Fernàndez, Jordi

AU - Irimia, Manuel

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.

UR - http://www.scopus.com/inward/record.url?scp=85035791355&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85035791355&partnerID=8YFLogxK

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 -