A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons

Research output: Contribution to journalArticlepeer-review

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A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons. / Torres-Mendez, Antonio; Bonnal, Sophie; Marquez, Yamile; Roth, Jonathan; Iglesias, Marta; Permanyer, Jon; Almundi, Isabel; O'Hanlon, Dave; Guitart, Tanit; Soller, Matthias; Gingras, Anne-Claude; Gebauer, Fátima; Rentzsch, Fabian; Blencowe, Benjamin J.; Valcárcel, Juan; Irimia, Manuel.

In: Nature Ecology and Evolution, Vol. 3, 2019, p. 691–701.

Research output: Contribution to journalArticlepeer-review

Harvard

Torres-Mendez, A, Bonnal, S, Marquez, Y, Roth, J, Iglesias, M, Permanyer, J, Almundi, I, O'Hanlon, D, Guitart, T, Soller, M, Gingras, A-C, Gebauer, F, Rentzsch, F, Blencowe, BJ, Valcárcel, J & Irimia, M 2019, 'A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons', Nature Ecology and Evolution, vol. 3, pp. 691–701. https://doi.org/10.1038/s41559-019-0813-6

APA

Torres-Mendez, A., Bonnal, S., Marquez, Y., Roth, J., Iglesias, M., Permanyer, J., Almundi, I., O'Hanlon, D., Guitart, T., Soller, M., Gingras, A-C., Gebauer, F., Rentzsch, F., Blencowe, B. J., Valcárcel, J., & Irimia, M. (2019). A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons. Nature Ecology and Evolution, 3, 691–701. https://doi.org/10.1038/s41559-019-0813-6

Vancouver

Author

Torres-Mendez, Antonio ; Bonnal, Sophie ; Marquez, Yamile ; Roth, Jonathan ; Iglesias, Marta ; Permanyer, Jon ; Almundi, Isabel ; O'Hanlon, Dave ; Guitart, Tanit ; Soller, Matthias ; Gingras, Anne-Claude ; Gebauer, Fátima ; Rentzsch, Fabian ; Blencowe, Benjamin J. ; Valcárcel, Juan ; Irimia, Manuel. / A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons. In: Nature Ecology and Evolution. 2019 ; Vol. 3. pp. 691–701.

Bibtex

@article{bbf1c3b3d5ba470d873ecfb0653ec197,
title = "A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons",
abstract = "The mechanisms by which entire programmes of gene regulation emerged during evolution are poorly understood. Neuronal microexons represent the most conserved class of alternative splicing in vertebrates, and are critical for proper brain development and function. Here, we discover neural microexon programmes in non-vertebrate species and trace their origin to bilaterian ancestors through the emergence of a previously uncharacterized {\textquoteleft}enhancer of microexons{\textquoteright} (eMIC) protein domain. The eMIC domain originated as an alternative, neural-enriched splice isoform of the pan-eukaryotic Srrm2/SRm300 splicing factor gene, and subsequently became fixed in the vertebrate and neuronal-specific splicing regulator Srrm4/nSR100 and its paralogue Srrm3. Remarkably, the eMIC domain is necessary and sufficient for microexon splicing, and functions by interacting with the earliest components required for exon recognition. The emergence of a novel domain with restricted expression in the nervous system thus resulted in the evolution of splicing programmes that qualitatively expanded the neuronal molecular complexity in bilaterians. ",
keywords = "complexity, genome evolution, transcriptomics, nervous system",
author = "Antonio Torres-Mendez and Sophie Bonnal and Yamile Marquez and Jonathan Roth and Marta Iglesias and Jon Permanyer and Isabel Almundi and Dave O'Hanlon and Tanit Guitart and Matthias Soller and Anne-Claude Gingras and F{\'a}tima Gebauer and Fabian Rentzsch and Blencowe, {Benjamin J.} and Juan Valc{\'a}rcel and Manuel Irimia",
year = "2019",
doi = "10.1038/s41559-019-0813-6",
language = "English",
volume = "3",
pages = "691–701",
journal = "Nature Ecology and Evolution",
issn = "2397-334X",
publisher = "Nature Publishing Group",

}

RIS

TY - JOUR

T1 - A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons

AU - Torres-Mendez, Antonio

AU - Bonnal, Sophie

AU - Marquez, Yamile

AU - Roth, Jonathan

AU - Iglesias, Marta

AU - Permanyer, Jon

AU - Almundi, Isabel

AU - O'Hanlon, Dave

AU - Guitart, Tanit

AU - Soller, Matthias

AU - Gingras, Anne-Claude

AU - Gebauer, Fátima

AU - Rentzsch, Fabian

AU - Blencowe, Benjamin J.

AU - Valcárcel, Juan

AU - Irimia, Manuel

PY - 2019

Y1 - 2019

N2 - The mechanisms by which entire programmes of gene regulation emerged during evolution are poorly understood. Neuronal microexons represent the most conserved class of alternative splicing in vertebrates, and are critical for proper brain development and function. Here, we discover neural microexon programmes in non-vertebrate species and trace their origin to bilaterian ancestors through the emergence of a previously uncharacterized ‘enhancer of microexons’ (eMIC) protein domain. The eMIC domain originated as an alternative, neural-enriched splice isoform of the pan-eukaryotic Srrm2/SRm300 splicing factor gene, and subsequently became fixed in the vertebrate and neuronal-specific splicing regulator Srrm4/nSR100 and its paralogue Srrm3. Remarkably, the eMIC domain is necessary and sufficient for microexon splicing, and functions by interacting with the earliest components required for exon recognition. The emergence of a novel domain with restricted expression in the nervous system thus resulted in the evolution of splicing programmes that qualitatively expanded the neuronal molecular complexity in bilaterians.

AB - The mechanisms by which entire programmes of gene regulation emerged during evolution are poorly understood. Neuronal microexons represent the most conserved class of alternative splicing in vertebrates, and are critical for proper brain development and function. Here, we discover neural microexon programmes in non-vertebrate species and trace their origin to bilaterian ancestors through the emergence of a previously uncharacterized ‘enhancer of microexons’ (eMIC) protein domain. The eMIC domain originated as an alternative, neural-enriched splice isoform of the pan-eukaryotic Srrm2/SRm300 splicing factor gene, and subsequently became fixed in the vertebrate and neuronal-specific splicing regulator Srrm4/nSR100 and its paralogue Srrm3. Remarkably, the eMIC domain is necessary and sufficient for microexon splicing, and functions by interacting with the earliest components required for exon recognition. The emergence of a novel domain with restricted expression in the nervous system thus resulted in the evolution of splicing programmes that qualitatively expanded the neuronal molecular complexity in bilaterians.

KW - complexity

KW - genome evolution

KW - transcriptomics

KW - nervous system

UR - http://www.scopus.com/inward/record.url?scp=85062469652&partnerID=8YFLogxK

U2 - 10.1038/s41559-019-0813-6

DO - 10.1038/s41559-019-0813-6

M3 - Article

VL - 3

SP - 691

EP - 701

JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

SN - 2397-334X

ER -