A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas
Proliferating cells need to coordinate cell division and growth to maintain size homeostasis. Any systematic deviation from a balance between growth and division results in progressive changes of cell size over subsequent generations. While most eukaryotic cells execute binary division after a mass...
| Main Authors: | , , , |
|---|---|
| Format: | Journal article |
| Published: |
Cold Spring Harbor Laboratory
2019
|
| _version_ | 1826297455514222592 |
|---|---|
| author | Heldt, F Tyson, J Cross, F Novák, B |
| author_facet | Heldt, F Tyson, J Cross, F Novák, B |
| author_sort | Heldt, F |
| collection | OXFORD |
| description | Proliferating cells need to coordinate cell division and growth to maintain size homeostasis. Any systematic deviation from a balance between growth and division results in progressive changes of cell size over subsequent generations. While most eukaryotic cells execute binary division after a mass doubling, the photosynthetic green alga Chlamydomonas can grow more than eight-fold during daytime before undergoing rapid cycles of DNA replication, mitosis and cell division at night, which produce up to 16 daughter cells. Here, we propose a mechanistic model for multiple fission and size control in Chlamydomonas . The model comprises a light-sensitive and size-dependent biochemical toggle switch that acts as a sizer and guards transitions into and exit from a phase of cell-division cycle oscillations. We show that this simple ‘sizer-oscillator’ arrangement reproduces the experimentally observed features of multiple-fission cycles and the response of Chlamydomonas cells to different light-dark regimes. Our model also makes testable predictions about the dynamical properties of the biochemical network that controls these features and about the network’s makeup. Collectively, these results provide a new perspective on the concept of a ‘commitment point’ during the growth of Chlamydomonas cells and hint at an intriguing continuity of cell-size control in different eukaryotic lineages. Graphical abstract <jats:fig fig-type="figure" id="ufig1" orientation="portrait" position="float"><jats:graphic orientation="portrait" position="float" xlink:href="648436v1_ufig1" xmlns:xlink="http://www.w3.org/1999/xlink"></jats:graphic> <jats:list list-type="bullet"><jats:list-item> G1-sizer and S/M-oscillator can give rise to multiple-fission cycles in Chlamydomonas <jats:list-item> Light-responsive bistable switch may guard transition between G1 and S/M-cycles <jats:list-item> Illumination increases S/M-entry threshold, causing multiple-fission cycles <jats:list-item> Dark shift lowers S/M-entry threshold, allowing small cells to commit to fewer divisions</jats:list-item></jats:list-item></jats:list-item></jats:list-item></jats:list></jats:fig> |
| first_indexed | 2024-03-07T04:31:53Z |
| format | Journal article |
| id | oxford-uuid:ce9c42a6-d181-4661-836d-00e1392cd8e7 |
| institution | University of Oxford |
| last_indexed | 2024-03-07T04:31:53Z |
| publishDate | 2019 |
| publisher | Cold Spring Harbor Laboratory |
| record_format | dspace |
| spelling | oxford-uuid:ce9c42a6-d181-4661-836d-00e1392cd8e72022-03-27T07:36:46ZA single light-responsive sizer can control multiple-fission cycles in ChlamydomonasJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:ce9c42a6-d181-4661-836d-00e1392cd8e7Symplectic Elements at OxfordCold Spring Harbor Laboratory2019Heldt, FTyson, JCross, FNovák, BProliferating cells need to coordinate cell division and growth to maintain size homeostasis. Any systematic deviation from a balance between growth and division results in progressive changes of cell size over subsequent generations. While most eukaryotic cells execute binary division after a mass doubling, the photosynthetic green alga Chlamydomonas can grow more than eight-fold during daytime before undergoing rapid cycles of DNA replication, mitosis and cell division at night, which produce up to 16 daughter cells. Here, we propose a mechanistic model for multiple fission and size control in Chlamydomonas . The model comprises a light-sensitive and size-dependent biochemical toggle switch that acts as a sizer and guards transitions into and exit from a phase of cell-division cycle oscillations. We show that this simple ‘sizer-oscillator’ arrangement reproduces the experimentally observed features of multiple-fission cycles and the response of Chlamydomonas cells to different light-dark regimes. Our model also makes testable predictions about the dynamical properties of the biochemical network that controls these features and about the network’s makeup. Collectively, these results provide a new perspective on the concept of a ‘commitment point’ during the growth of Chlamydomonas cells and hint at an intriguing continuity of cell-size control in different eukaryotic lineages. Graphical abstract <jats:fig fig-type="figure" id="ufig1" orientation="portrait" position="float"><jats:graphic orientation="portrait" position="float" xlink:href="648436v1_ufig1" xmlns:xlink="http://www.w3.org/1999/xlink"></jats:graphic> <jats:list list-type="bullet"><jats:list-item> G1-sizer and S/M-oscillator can give rise to multiple-fission cycles in Chlamydomonas <jats:list-item> Light-responsive bistable switch may guard transition between G1 and S/M-cycles <jats:list-item> Illumination increases S/M-entry threshold, causing multiple-fission cycles <jats:list-item> Dark shift lowers S/M-entry threshold, allowing small cells to commit to fewer divisions</jats:list-item></jats:list-item></jats:list-item></jats:list-item></jats:list></jats:fig> |
| spellingShingle | Heldt, F Tyson, J Cross, F Novák, B A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas |
| title | A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas |
| title_full | A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas |
| title_fullStr | A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas |
| title_full_unstemmed | A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas |
| title_short | A single light-responsive sizer can control multiple-fission cycles in Chlamydomonas |
| title_sort | single light responsive sizer can control multiple fission cycles in chlamydomonas |
| work_keys_str_mv | AT heldtf asinglelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas AT tysonj asinglelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas AT crossf asinglelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas AT novakb asinglelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas AT heldtf singlelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas AT tysonj singlelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas AT crossf singlelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas AT novakb singlelightresponsivesizercancontrolmultiplefissioncyclesinchlamydomonas |