Cargando…

Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos

BACKGROUND: Recently, much progress has been made in the field of gene-expression in early embryogenesis. However, the dynamic behaviour of transcriptomes in individual embryos has hardly been studied yet and the time points at which pools of embryos are collected are usually still quite far apart....

Descripción completa

Detalles Bibliográficos
Autores principales: Rauwerda, Han, Pagano, Johanna F. B., de Leeuw, Wim C., Ensink, Wim, Nehrdich, Ulrike, de Jong, Mark, Jonker, Martijs, Spaink, Herman P., Breit, Timo M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5387192/
https://www.ncbi.nlm.nih.gov/pubmed/28399811
http://dx.doi.org/10.1186/s12864-017-3672-z
_version_ 1782520894719000576
author Rauwerda, Han
Pagano, Johanna F. B.
de Leeuw, Wim C.
Ensink, Wim
Nehrdich, Ulrike
de Jong, Mark
Jonker, Martijs
Spaink, Herman P.
Breit, Timo M.
author_facet Rauwerda, Han
Pagano, Johanna F. B.
de Leeuw, Wim C.
Ensink, Wim
Nehrdich, Ulrike
de Jong, Mark
Jonker, Martijs
Spaink, Herman P.
Breit, Timo M.
author_sort Rauwerda, Han
collection PubMed
description BACKGROUND: Recently, much progress has been made in the field of gene-expression in early embryogenesis. However, the dynamic behaviour of transcriptomes in individual embryos has hardly been studied yet and the time points at which pools of embryos are collected are usually still quite far apart. Here, we present a high-resolution gene-expression time series with 180 individual zebrafish embryos, obtained from nine different spawns, developmentally ordered and profiled from late blastula to mid-gastrula stage. On average one embryo per minute was analysed. The focus was on identification and description of the transcriptome dynamics of the expressed genes in this embryonic stage, rather than to biologically interpret profiles in cellular processes and pathways. RESULTS: In the late blastula to mid-gastrula stage, we found 6,734 genes being expressed with low variability and rather gradual changes. Ten types of dynamic behaviour were defined, such as genes with continuously increasing or decreasing expression, and all expressed genes were grouped into these types. Also, the exact expression starting and stopping points of several hundred genes during this developmental period could be pinpointed. Although the resolution of the experiment was so high, that we were able to clearly identify four known oscillating genes, no genes were observed with a peaking expression. Additionally, several genes showed expression at two or three distinct levels that strongly related to the spawn an embryo originated from. CONCLUSION: Our unique experimental set-up of whole-transcriptome analysis of 180 individual embryos, provided an unparalleled in-depth insight into the dynamics of early zebrafish embryogenesis. The existence of a tightly regulated embryonic transcriptome program, even between individuals from different spawns is shown. We have made the expression profile of all genes available for domain experts. The fact that we were able to separate the different spawns by their gene-expression variance over all expressed genes, underlines the importance of spawn specificity, as well as the unexpectedly tight gene-expression regulation in early zebrafish embryogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3672-z) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5387192
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-53871922017-04-11 Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos Rauwerda, Han Pagano, Johanna F. B. de Leeuw, Wim C. Ensink, Wim Nehrdich, Ulrike de Jong, Mark Jonker, Martijs Spaink, Herman P. Breit, Timo M. BMC Genomics Research Article BACKGROUND: Recently, much progress has been made in the field of gene-expression in early embryogenesis. However, the dynamic behaviour of transcriptomes in individual embryos has hardly been studied yet and the time points at which pools of embryos are collected are usually still quite far apart. Here, we present a high-resolution gene-expression time series with 180 individual zebrafish embryos, obtained from nine different spawns, developmentally ordered and profiled from late blastula to mid-gastrula stage. On average one embryo per minute was analysed. The focus was on identification and description of the transcriptome dynamics of the expressed genes in this embryonic stage, rather than to biologically interpret profiles in cellular processes and pathways. RESULTS: In the late blastula to mid-gastrula stage, we found 6,734 genes being expressed with low variability and rather gradual changes. Ten types of dynamic behaviour were defined, such as genes with continuously increasing or decreasing expression, and all expressed genes were grouped into these types. Also, the exact expression starting and stopping points of several hundred genes during this developmental period could be pinpointed. Although the resolution of the experiment was so high, that we were able to clearly identify four known oscillating genes, no genes were observed with a peaking expression. Additionally, several genes showed expression at two or three distinct levels that strongly related to the spawn an embryo originated from. CONCLUSION: Our unique experimental set-up of whole-transcriptome analysis of 180 individual embryos, provided an unparalleled in-depth insight into the dynamics of early zebrafish embryogenesis. The existence of a tightly regulated embryonic transcriptome program, even between individuals from different spawns is shown. We have made the expression profile of all genes available for domain experts. The fact that we were able to separate the different spawns by their gene-expression variance over all expressed genes, underlines the importance of spawn specificity, as well as the unexpectedly tight gene-expression regulation in early zebrafish embryogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3672-z) contains supplementary material, which is available to authorized users. BioMed Central 2017-04-11 /pmc/articles/PMC5387192/ /pubmed/28399811 http://dx.doi.org/10.1186/s12864-017-3672-z Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Rauwerda, Han
Pagano, Johanna F. B.
de Leeuw, Wim C.
Ensink, Wim
Nehrdich, Ulrike
de Jong, Mark
Jonker, Martijs
Spaink, Herman P.
Breit, Timo M.
Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos
title Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos
title_full Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos
title_fullStr Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos
title_full_unstemmed Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos
title_short Transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos
title_sort transcriptome dynamics in early zebrafish embryogenesis determined by high-resolution time course analysis of 180 successive, individual zebrafish embryos
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5387192/
https://www.ncbi.nlm.nih.gov/pubmed/28399811
http://dx.doi.org/10.1186/s12864-017-3672-z
work_keys_str_mv AT rauwerdahan transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT paganojohannafb transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT deleeuwwimc transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT ensinkwim transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT nehrdichulrike transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT dejongmark transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT jonkermartijs transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT spainkhermanp transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos
AT breittimom transcriptomedynamicsinearlyzebrafishembryogenesisdeterminedbyhighresolutiontimecourseanalysisof180successiveindividualzebrafishembryos