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

Petrosino, G.; Ponte, G.; Volpe, M.; Zarrella, I.; Langella, C.; Di Cristina, G.; Finaurini, S.; Russo, M. T.; Basu, S.; Musacchia, F.; Ristoratore, F.; Pavlinic, D.; Benes, V.; Ferrante, M. I.; Albertin, C.; Simakov, O.; Gustincich, S.; Fiorito, G.; Sanges, R.

doi:10.1101/2021.01.24.427974

bioRxiv · 10.1101/2021.01.24.427974

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

Petrosino, G.·Ponte, G.·Volpe, M.·Zarrella, I.·Langella, C.·Di Cristina, G.·Finaurini, S.·Russo, M. T.·Basu, S.·Musacchia, F.·Ristoratore, F.·Pavlinic, D.·Benes, V.·Ferrante, M. I.·Albertin, C.·Simakov, O.·Gustincich, S.·Fiorito, G.·Sanges, R.

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Abstract

BackgroundTransposable elements (TEs) widely contributed 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 of full-length transpositionally competent TEs has not been performed in this genus. ResultsHere we report the identification of LINE elements competent for retrotransposition in Octopus vulgaris and Octopus bimaculoides and show evidence suggesting that they might be active driving germline polymorphisms among individuals and somatic polymorphisms 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. ConclusionsThe neural transcriptome of the octopus shows the transcription of thousands of putative lncRNAs and of a full lenght 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.

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Petrosino, G., Ponte, G., Volpe, M., Zarrella, I., Langella, C., Di Cristina, G., Finaurini, S., Russo, M. T., Basu, S., Musacchia, F., Ristoratore, F., Pavlinic, D., Benes, V., Ferrante, M. I., Albertin, C., Simakov, O., Gustincich, S., Fiorito, G., Sanges, R.. 2021-01-25. Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain. https://doi.org/10.1101/2021.01.24.427974

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