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The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios

BACKGROUND: Planarians can regenerate entire animals from a small fragment of the body. The regenerating fragment is able to create new tissues and remodel existing tissues to form a complete animal. Thus different fragments with very different starting components eventually converge on the same sol...

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Autores principales: Kao, Damian, Felix, Daniel, Aboobaker, Aziz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4046745/
https://www.ncbi.nlm.nih.gov/pubmed/24238224
http://dx.doi.org/10.1186/1471-2164-14-797
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author Kao, Damian
Felix, Daniel
Aboobaker, Aziz
author_facet Kao, Damian
Felix, Daniel
Aboobaker, Aziz
author_sort Kao, Damian
collection PubMed
description BACKGROUND: Planarians can regenerate entire animals from a small fragment of the body. The regenerating fragment is able to create new tissues and remodel existing tissues to form a complete animal. Thus different fragments with very different starting components eventually converge on the same solution. In this study, we performed an extensive RNA-seq time-course on regenerating head and tail fragments to observe the differences and similarities of the transcriptional landscape between head and tail fragments during regeneration. RESULTS: We have consolidated existing transcriptomic data for S. mediterranea to generate a high confidence set of transcripts for use in genome wide expression studies. We performed a RNA-seq time-course on regenerating head and tail fragments from 0 hours to 3 days. We found that the transcriptome profiles of head and tail regeneration were very different at the start of regeneration; however, an unexpected convergence of transcriptional profiles occurred at 48 hours when head and tail fragments are still morphologically distinct. By comparing differentially expressed transcripts at various time-points, we revealed that this divergence/convergence pattern is caused by a shared regulatory program that runs early in heads and later in tails. Additionally, we also performed RNA-seq on smed-prep(RNAi) tail fragments which ultimately fail to regenerate anterior structures. We find the gene regulation program in response to smed-prep(RNAi) to display the opposite regulatory trend compared to the previously mentioned share regulatory program during regeneration. Using annotation data and comparative approaches, we also identified a set of approximately 4,800 triclad specific transcripts that were enriched amongst the genes displaying differential expression during the regeneration time-course. CONCLUSION: The regeneration transcriptome of head and tail regeneration provides us with a rich resource for investigating the global expression changes that occurs during regeneration. We show that very different regenerative scenarios utilize a shared core regenerative program. Furthermore, our consolidated transcriptome and annotations allowed us to identity triclad specific transcripts that are enriched within this core regulatory program. Our data support the hypothesis that both conserved aspects of animal developmental programs and recent evolutionarily innovations work in concert to control regeneration. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-14-797) contains supplementary material, which is available to authorized users.
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spelling pubmed-40467452014-06-06 The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios Kao, Damian Felix, Daniel Aboobaker, Aziz BMC Genomics Research Article BACKGROUND: Planarians can regenerate entire animals from a small fragment of the body. The regenerating fragment is able to create new tissues and remodel existing tissues to form a complete animal. Thus different fragments with very different starting components eventually converge on the same solution. In this study, we performed an extensive RNA-seq time-course on regenerating head and tail fragments to observe the differences and similarities of the transcriptional landscape between head and tail fragments during regeneration. RESULTS: We have consolidated existing transcriptomic data for S. mediterranea to generate a high confidence set of transcripts for use in genome wide expression studies. We performed a RNA-seq time-course on regenerating head and tail fragments from 0 hours to 3 days. We found that the transcriptome profiles of head and tail regeneration were very different at the start of regeneration; however, an unexpected convergence of transcriptional profiles occurred at 48 hours when head and tail fragments are still morphologically distinct. By comparing differentially expressed transcripts at various time-points, we revealed that this divergence/convergence pattern is caused by a shared regulatory program that runs early in heads and later in tails. Additionally, we also performed RNA-seq on smed-prep(RNAi) tail fragments which ultimately fail to regenerate anterior structures. We find the gene regulation program in response to smed-prep(RNAi) to display the opposite regulatory trend compared to the previously mentioned share regulatory program during regeneration. Using annotation data and comparative approaches, we also identified a set of approximately 4,800 triclad specific transcripts that were enriched amongst the genes displaying differential expression during the regeneration time-course. CONCLUSION: The regeneration transcriptome of head and tail regeneration provides us with a rich resource for investigating the global expression changes that occurs during regeneration. We show that very different regenerative scenarios utilize a shared core regenerative program. Furthermore, our consolidated transcriptome and annotations allowed us to identity triclad specific transcripts that are enriched within this core regulatory program. Our data support the hypothesis that both conserved aspects of animal developmental programs and recent evolutionarily innovations work in concert to control regeneration. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-14-797) contains supplementary material, which is available to authorized users. BioMed Central 2013-11-16 /pmc/articles/PMC4046745/ /pubmed/24238224 http://dx.doi.org/10.1186/1471-2164-14-797 Text en © Kao et al.; licensee BioMed Central Ltd. 2013 This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Kao, Damian
Felix, Daniel
Aboobaker, Aziz
The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios
title The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios
title_full The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios
title_fullStr The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios
title_full_unstemmed The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios
title_short The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios
title_sort planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4046745/
https://www.ncbi.nlm.nih.gov/pubmed/24238224
http://dx.doi.org/10.1186/1471-2164-14-797
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