Control of tissue development and cell diversity by cell cycle-dependent transcriptional filtering
Cell cycle duration changes dramatically during development, starting out fast to generate cells quickly and slowing down over time as the organism matures. The cell cycle can also act as a transcriptional filter to control the expression of long gene transcripts, which are partially transcribed in...
Main Authors: | , , , |
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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2021-07-01
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Series: | eLife |
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Online Access: | https://elifesciences.org/articles/64951 |
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author | Maria Abou Chakra Ruth Isserlin Thinh N Tran Gary D Bader |
author_facet | Maria Abou Chakra Ruth Isserlin Thinh N Tran Gary D Bader |
author_sort | Maria Abou Chakra |
collection | DOAJ |
description | Cell cycle duration changes dramatically during development, starting out fast to generate cells quickly and slowing down over time as the organism matures. The cell cycle can also act as a transcriptional filter to control the expression of long gene transcripts, which are partially transcribed in short cycles. Using mathematical simulations of cell proliferation, we identify an emergent property that this filter can act as a tuning knob to control gene transcript expression, cell diversity, and the number and proportion of different cell types in a tissue. Our predictions are supported by comparison to single-cell RNA-seq data captured over embryonic development. Additionally, evolutionary genome analysis shows that fast-developing organisms have a narrow genomic distribution of gene lengths while slower developers have an expanded number of long genes. Our results support the idea that cell cycle dynamics may be important across multicellular animals for controlling gene transcript expression and cell fate. |
first_indexed | 2024-04-11T10:33:47Z |
format | Article |
id | doaj.art-94c58a5523a7488fb18bc1d4bc928c83 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-11T10:33:47Z |
publishDate | 2021-07-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
spelling | doaj.art-94c58a5523a7488fb18bc1d4bc928c832022-12-22T04:29:21ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.64951Control of tissue development and cell diversity by cell cycle-dependent transcriptional filteringMaria Abou Chakra0https://orcid.org/0000-0002-4895-954XRuth Isserlin1Thinh N Tran2Gary D Bader3https://orcid.org/0000-0003-0185-8861The Donnelly Centre, University of Toronto, Toronto, CanadaThe Donnelly Centre, University of Toronto, Toronto, CanadaThe Donnelly Centre, University of Toronto, Toronto, CanadaThe Donnelly Centre, University of Toronto, Toronto, CanadaCell cycle duration changes dramatically during development, starting out fast to generate cells quickly and slowing down over time as the organism matures. The cell cycle can also act as a transcriptional filter to control the expression of long gene transcripts, which are partially transcribed in short cycles. Using mathematical simulations of cell proliferation, we identify an emergent property that this filter can act as a tuning knob to control gene transcript expression, cell diversity, and the number and proportion of different cell types in a tissue. Our predictions are supported by comparison to single-cell RNA-seq data captured over embryonic development. Additionally, evolutionary genome analysis shows that fast-developing organisms have a narrow genomic distribution of gene lengths while slower developers have an expanded number of long genes. Our results support the idea that cell cycle dynamics may be important across multicellular animals for controlling gene transcript expression and cell fate.https://elifesciences.org/articles/64951eukaryotescomputational modelcell cycle durationtranscriptional filterfate decisionsearly development |
spellingShingle | Maria Abou Chakra Ruth Isserlin Thinh N Tran Gary D Bader Control of tissue development and cell diversity by cell cycle-dependent transcriptional filtering eLife eukaryotes computational model cell cycle duration transcriptional filter fate decisions early development |
title | Control of tissue development and cell diversity by cell cycle-dependent transcriptional filtering |
title_full | Control of tissue development and cell diversity by cell cycle-dependent transcriptional filtering |
title_fullStr | Control of tissue development and cell diversity by cell cycle-dependent transcriptional filtering |
title_full_unstemmed | Control of tissue development and cell diversity by cell cycle-dependent transcriptional filtering |
title_short | Control of tissue development and cell diversity by cell cycle-dependent transcriptional filtering |
title_sort | control of tissue development and cell diversity by cell cycle dependent transcriptional filtering |
topic | eukaryotes computational model cell cycle duration transcriptional filter fate decisions early development |
url | https://elifesciences.org/articles/64951 |
work_keys_str_mv | AT mariaabouchakra controloftissuedevelopmentandcelldiversitybycellcycledependenttranscriptionalfiltering AT ruthisserlin controloftissuedevelopmentandcelldiversitybycellcycledependenttranscriptionalfiltering AT thinhntran controloftissuedevelopmentandcelldiversitybycellcycledependenttranscriptionalfiltering AT garydbader controloftissuedevelopmentandcelldiversitybycellcycledependenttranscriptionalfiltering |