Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery.
Progression through the cell cycle in eukaryotes is regulated on multiple levels. The main driver of the cell cycle progression is the periodic activity of cyclin-dependent kinase (CDK) complexes. In parallel, transcription during the cell cycle is regulated by a transcriptional program that ensures...
Main Authors: | , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Public Library of Science (PLoS)
2020-03-01
|
Series: | PLoS Genetics |
Online Access: | https://doi.org/10.1371/journal.pgen.1008584 |
id |
doaj-9102e67c91534c61934e29db7aebbfde |
---|---|
record_format |
Article |
spelling |
doaj-9102e67c91534c61934e29db7aebbfde2021-04-21T13:51:26ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042020-03-01163e100858410.1371/journal.pgen.1008584Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery.Alberto Pérez-PosadaOmaya DudinEduard Ocaña-PallarèsIñaki Ruiz-TrilloAndrej OndrackaProgression through the cell cycle in eukaryotes is regulated on multiple levels. The main driver of the cell cycle progression is the periodic activity of cyclin-dependent kinase (CDK) complexes. In parallel, transcription during the cell cycle is regulated by a transcriptional program that ensures the just-in-time gene expression. Many core cell cycle regulators are widely conserved in eukaryotes, among them cyclins and CDKs; however, periodic transcriptional programs are divergent between distantly related species. In addition, many otherwise conserved cell cycle regulators have been lost and independently evolved in yeast, a widely used model organism for cell cycle research. For a better understanding of the evolution of the cell cycle regulation in opisthokonts, we investigated the transcriptional program during the cell cycle of the filasterean Capsaspora owczarzaki, a unicellular species closely related to animals. We developed a protocol for cell cycle synchronization in Capsaspora cultures and assessed gene expression over time across the entire cell cycle. We identified a set of 801 periodic genes that grouped into five clusters of expression over time. Comparison with datasets from other eukaryotes revealed that the periodic transcriptional program of Capsaspora is most similar to that of animal cells. We found that orthologues of cyclin A, B and E are expressed at the same cell cycle stages as in human cells and in the same temporal order. However, in contrast to human cells where these cyclins interact with multiple CDKs, Capsaspora cyclins likely interact with a single ancestral CDK1-3. Thus, the Capsaspora cyclin-CDK system could represent an intermediate state in the evolution of animal-like cyclin-CDK regulation. Overall, our results demonstrate that Capsaspora could be a useful unicellular model system for animal cell cycle regulation.https://doi.org/10.1371/journal.pgen.1008584 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Alberto Pérez-Posada Omaya Dudin Eduard Ocaña-Pallarès Iñaki Ruiz-Trillo Andrej Ondracka |
spellingShingle |
Alberto Pérez-Posada Omaya Dudin Eduard Ocaña-Pallarès Iñaki Ruiz-Trillo Andrej Ondracka Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery. PLoS Genetics |
author_facet |
Alberto Pérez-Posada Omaya Dudin Eduard Ocaña-Pallarès Iñaki Ruiz-Trillo Andrej Ondracka |
author_sort |
Alberto Pérez-Posada |
title |
Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery. |
title_short |
Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery. |
title_full |
Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery. |
title_fullStr |
Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery. |
title_full_unstemmed |
Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery. |
title_sort |
cell cycle transcriptomics of capsaspora provides insights into the evolution of cyclin-cdk machinery. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS Genetics |
issn |
1553-7390 1553-7404 |
publishDate |
2020-03-01 |
description |
Progression through the cell cycle in eukaryotes is regulated on multiple levels. The main driver of the cell cycle progression is the periodic activity of cyclin-dependent kinase (CDK) complexes. In parallel, transcription during the cell cycle is regulated by a transcriptional program that ensures the just-in-time gene expression. Many core cell cycle regulators are widely conserved in eukaryotes, among them cyclins and CDKs; however, periodic transcriptional programs are divergent between distantly related species. In addition, many otherwise conserved cell cycle regulators have been lost and independently evolved in yeast, a widely used model organism for cell cycle research. For a better understanding of the evolution of the cell cycle regulation in opisthokonts, we investigated the transcriptional program during the cell cycle of the filasterean Capsaspora owczarzaki, a unicellular species closely related to animals. We developed a protocol for cell cycle synchronization in Capsaspora cultures and assessed gene expression over time across the entire cell cycle. We identified a set of 801 periodic genes that grouped into five clusters of expression over time. Comparison with datasets from other eukaryotes revealed that the periodic transcriptional program of Capsaspora is most similar to that of animal cells. We found that orthologues of cyclin A, B and E are expressed at the same cell cycle stages as in human cells and in the same temporal order. However, in contrast to human cells where these cyclins interact with multiple CDKs, Capsaspora cyclins likely interact with a single ancestral CDK1-3. Thus, the Capsaspora cyclin-CDK system could represent an intermediate state in the evolution of animal-like cyclin-CDK regulation. Overall, our results demonstrate that Capsaspora could be a useful unicellular model system for animal cell cycle regulation. |
url |
https://doi.org/10.1371/journal.pgen.1008584 |
work_keys_str_mv |
AT albertoperezposada cellcycletranscriptomicsofcapsasporaprovidesinsightsintotheevolutionofcyclincdkmachinery AT omayadudin cellcycletranscriptomicsofcapsasporaprovidesinsightsintotheevolutionofcyclincdkmachinery AT eduardocanapallares cellcycletranscriptomicsofcapsasporaprovidesinsightsintotheevolutionofcyclincdkmachinery AT inakiruiztrillo cellcycletranscriptomicsofcapsasporaprovidesinsightsintotheevolutionofcyclincdkmachinery AT andrejondracka cellcycletranscriptomicsofcapsasporaprovidesinsightsintotheevolutionofcyclincdkmachinery |
_version_ |
1714668684582060032 |