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Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain

BACKGROUND: Transposable elements (TEs) widely contribute to the evolution of genomes allowing genomic innovations, generating germinal and somatic heterogeneity, and giving birth to long non-coding RNAs (lncRNAs). These features have been associated to the evolution, functioning, and complexity of...

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Autores principales: Petrosino, Giuseppe, Ponte, Giovanna, Volpe, Massimiliano, Zarrella, Ilaria, Ansaloni, Federico, Langella, Concetta, Di Cristina, Giulia, Finaurini, Sara, Russo, Monia T., Basu, Swaraj, Musacchia, Francesco, Ristoratore, Filomena, Pavlinic, Dinko, Benes, Vladimir, Ferrante, Maria I., Albertin, Caroline, Simakov, Oleg, Gustincich, Stefano, Fiorito, Graziano, Sanges, Remo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9115989/
https://www.ncbi.nlm.nih.gov/pubmed/35581640
http://dx.doi.org/10.1186/s12915-022-01303-5
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author Petrosino, Giuseppe
Ponte, Giovanna
Volpe, Massimiliano
Zarrella, Ilaria
Ansaloni, Federico
Langella, Concetta
Di Cristina, Giulia
Finaurini, Sara
Russo, Monia T.
Basu, Swaraj
Musacchia, Francesco
Ristoratore, Filomena
Pavlinic, Dinko
Benes, Vladimir
Ferrante, Maria I.
Albertin, Caroline
Simakov, Oleg
Gustincich, Stefano
Fiorito, Graziano
Sanges, Remo
author_facet Petrosino, Giuseppe
Ponte, Giovanna
Volpe, Massimiliano
Zarrella, Ilaria
Ansaloni, Federico
Langella, Concetta
Di Cristina, Giulia
Finaurini, Sara
Russo, Monia T.
Basu, Swaraj
Musacchia, Francesco
Ristoratore, Filomena
Pavlinic, Dinko
Benes, Vladimir
Ferrante, Maria I.
Albertin, Caroline
Simakov, Oleg
Gustincich, Stefano
Fiorito, Graziano
Sanges, Remo
author_sort Petrosino, Giuseppe
collection PubMed
description BACKGROUND: Transposable elements (TEs) widely contribute to the evolution of genomes allowing genomic innovations, generating germinal and somatic heterogeneity, and giving birth to long non-coding RNAs (lncRNAs). These features have been associated to the evolution, functioning, and complexity of the nervous system at such a level that somatic retrotransposition of long interspersed element (LINE) L1 has been proposed to be associated to human cognition. Among invertebrates, octopuses are fascinating animals whose nervous system reaches a high level of complexity achieving sophisticated cognitive abilities. The sequencing of the genome of the Octopus bimaculoides revealed a striking expansion of TEs which were proposed to have contributed to the evolution of its complex nervous system. We recently found a similar expansion also in the genome of Octopus vulgaris. However, a specific search for the existence and the transcription of full-length transpositionally competent TEs has not been performed in this genus. RESULTS: Here, we report the identification of LINE elements competent for retrotransposition in Octopus vulgaris and Octopus bimaculoides and show evidence suggesting that they might be transcribed and determine germline and somatic polymorphisms especially in the brain. Transcription and translation measured for one of these elements resulted in specific signals in neurons belonging to areas associated with behavioral plasticity. We also report the transcription of thousands of lncRNAs and the pervasive inclusion of TE fragments in the transcriptomes of both Octopus species, further testifying the crucial activity of TEs in the evolution of the octopus genomes. CONCLUSIONS: The neural transcriptome of the octopus shows the transcription of thousands of putative lncRNAs and of a full-length LINE element belonging to the RTE class. We speculate that a convergent evolutionary process involving retrotransposons activity in the brain has been important for the evolution of sophisticated cognitive abilities in this genus. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01303-5.
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spelling pubmed-91159892022-05-19 Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain Petrosino, Giuseppe Ponte, Giovanna Volpe, Massimiliano Zarrella, Ilaria Ansaloni, Federico Langella, Concetta Di Cristina, Giulia Finaurini, Sara Russo, Monia T. Basu, Swaraj Musacchia, Francesco Ristoratore, Filomena Pavlinic, Dinko Benes, Vladimir Ferrante, Maria I. Albertin, Caroline Simakov, Oleg Gustincich, Stefano Fiorito, Graziano Sanges, Remo BMC Biol Research Article BACKGROUND: Transposable elements (TEs) widely contribute to the evolution of genomes allowing genomic innovations, generating germinal and somatic heterogeneity, and giving birth to long non-coding RNAs (lncRNAs). These features have been associated to the evolution, functioning, and complexity of the nervous system at such a level that somatic retrotransposition of long interspersed element (LINE) L1 has been proposed to be associated to human cognition. Among invertebrates, octopuses are fascinating animals whose nervous system reaches a high level of complexity achieving sophisticated cognitive abilities. The sequencing of the genome of the Octopus bimaculoides revealed a striking expansion of TEs which were proposed to have contributed to the evolution of its complex nervous system. We recently found a similar expansion also in the genome of Octopus vulgaris. However, a specific search for the existence and the transcription of full-length transpositionally competent TEs has not been performed in this genus. RESULTS: Here, we report the identification of LINE elements competent for retrotransposition in Octopus vulgaris and Octopus bimaculoides and show evidence suggesting that they might be transcribed and determine germline and somatic polymorphisms especially in the brain. Transcription and translation measured for one of these elements resulted in specific signals in neurons belonging to areas associated with behavioral plasticity. We also report the transcription of thousands of lncRNAs and the pervasive inclusion of TE fragments in the transcriptomes of both Octopus species, further testifying the crucial activity of TEs in the evolution of the octopus genomes. CONCLUSIONS: The neural transcriptome of the octopus shows the transcription of thousands of putative lncRNAs and of a full-length LINE element belonging to the RTE class. We speculate that a convergent evolutionary process involving retrotransposons activity in the brain has been important for the evolution of sophisticated cognitive abilities in this genus. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01303-5. BioMed Central 2022-05-18 /pmc/articles/PMC9115989/ /pubmed/35581640 http://dx.doi.org/10.1186/s12915-022-01303-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Petrosino, Giuseppe
Ponte, Giovanna
Volpe, Massimiliano
Zarrella, Ilaria
Ansaloni, Federico
Langella, Concetta
Di Cristina, Giulia
Finaurini, Sara
Russo, Monia T.
Basu, Swaraj
Musacchia, Francesco
Ristoratore, Filomena
Pavlinic, Dinko
Benes, Vladimir
Ferrante, Maria I.
Albertin, Caroline
Simakov, Oleg
Gustincich, Stefano
Fiorito, Graziano
Sanges, Remo
Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
title Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
title_full Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
title_fullStr Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
title_full_unstemmed Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
title_short Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
title_sort identification of line retrotransposons and long non-coding rnas expressed in the octopus brain
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9115989/
https://www.ncbi.nlm.nih.gov/pubmed/35581640
http://dx.doi.org/10.1186/s12915-022-01303-5
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