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Transcriptional milestones in Dictyostelium development

Dictyostelium development begins with single-cell starvation and ends with multicellular fruiting bodies. Developmental morphogenesis is accompanied by sweeping transcriptional changes, encompassing nearly half of the 13,000 genes in the genome. We performed time-series RNA-sequencing analyses of th...

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Autores principales: Katoh-Kurasawa, Mariko, Hrovatin, Karin, Hirose, Shigenori, Webb, Amanda, Ho, Hsing-I, Zupan, Blaž, Shaulsky, Gad
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8327917/
https://www.ncbi.nlm.nih.gov/pubmed/34183452
http://dx.doi.org/10.1101/gr.275496.121
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author Katoh-Kurasawa, Mariko
Hrovatin, Karin
Hirose, Shigenori
Webb, Amanda
Ho, Hsing-I
Zupan, Blaž
Shaulsky, Gad
author_facet Katoh-Kurasawa, Mariko
Hrovatin, Karin
Hirose, Shigenori
Webb, Amanda
Ho, Hsing-I
Zupan, Blaž
Shaulsky, Gad
author_sort Katoh-Kurasawa, Mariko
collection PubMed
description Dictyostelium development begins with single-cell starvation and ends with multicellular fruiting bodies. Developmental morphogenesis is accompanied by sweeping transcriptional changes, encompassing nearly half of the 13,000 genes in the genome. We performed time-series RNA-sequencing analyses of the wild type and 20 mutants to explore the relationships between transcription and morphogenesis. These strains show developmental arrest at different stages, accelerated development, or atypical morphologies. Considering eight major morphological transitions, we identified 1371 milestone genes whose expression changes sharply between consecutive transitions. We also identified 1099 genes as members of 21 regulons, which are groups of genes that remain coordinately regulated despite the genetic, temporal, and developmental perturbations. The gene annotations in these groups validate known transitions and reveal new developmental events. For example, DNA replication genes are tightly coregulated with cell division genes, so they are expressed in mid-development although chromosomal DNA is not replicated. Our data set includes 486 transcriptional profiles that can help identify new relationships between transcription and development and improve gene annotations. We show its utility by showing that cycles of aggregation and disaggregation in allorecognition-defective mutants involve dedifferentiation. We also show sensitivity to genetic and developmental conditions in two commonly used actin genes, act6 and act15, and robustness of the coaA gene. Finally, we propose that gpdA is a better mRNA quantitation standard because it is less sensitive to external conditions than commonly used standards. The data set is available for democratized exploration through the web application dictyExpress and the data mining environment Orange.
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spelling pubmed-83279172022-02-01 Transcriptional milestones in Dictyostelium development Katoh-Kurasawa, Mariko Hrovatin, Karin Hirose, Shigenori Webb, Amanda Ho, Hsing-I Zupan, Blaž Shaulsky, Gad Genome Res Resource Dictyostelium development begins with single-cell starvation and ends with multicellular fruiting bodies. Developmental morphogenesis is accompanied by sweeping transcriptional changes, encompassing nearly half of the 13,000 genes in the genome. We performed time-series RNA-sequencing analyses of the wild type and 20 mutants to explore the relationships between transcription and morphogenesis. These strains show developmental arrest at different stages, accelerated development, or atypical morphologies. Considering eight major morphological transitions, we identified 1371 milestone genes whose expression changes sharply between consecutive transitions. We also identified 1099 genes as members of 21 regulons, which are groups of genes that remain coordinately regulated despite the genetic, temporal, and developmental perturbations. The gene annotations in these groups validate known transitions and reveal new developmental events. For example, DNA replication genes are tightly coregulated with cell division genes, so they are expressed in mid-development although chromosomal DNA is not replicated. Our data set includes 486 transcriptional profiles that can help identify new relationships between transcription and development and improve gene annotations. We show its utility by showing that cycles of aggregation and disaggregation in allorecognition-defective mutants involve dedifferentiation. We also show sensitivity to genetic and developmental conditions in two commonly used actin genes, act6 and act15, and robustness of the coaA gene. Finally, we propose that gpdA is a better mRNA quantitation standard because it is less sensitive to external conditions than commonly used standards. The data set is available for democratized exploration through the web application dictyExpress and the data mining environment Orange. Cold Spring Harbor Laboratory Press 2021-08 /pmc/articles/PMC8327917/ /pubmed/34183452 http://dx.doi.org/10.1101/gr.275496.121 Text en © 2021 Katoh-Kurasawa et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by-nc/4.0/This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) .
spellingShingle Resource
Katoh-Kurasawa, Mariko
Hrovatin, Karin
Hirose, Shigenori
Webb, Amanda
Ho, Hsing-I
Zupan, Blaž
Shaulsky, Gad
Transcriptional milestones in Dictyostelium development
title Transcriptional milestones in Dictyostelium development
title_full Transcriptional milestones in Dictyostelium development
title_fullStr Transcriptional milestones in Dictyostelium development
title_full_unstemmed Transcriptional milestones in Dictyostelium development
title_short Transcriptional milestones in Dictyostelium development
title_sort transcriptional milestones in dictyostelium development
topic Resource
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8327917/
https://www.ncbi.nlm.nih.gov/pubmed/34183452
http://dx.doi.org/10.1101/gr.275496.121
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