Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance.
Stem cell maintenance in multilayered shoot apical meristems (SAMs) of plants requires strict regulation of cell growth and division. Exactly how the complex milieu of chemical and mechanical signals interact in the central region of the SAM to regulate cell division plane orientation is not well un...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2022-06-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://doi.org/10.1371/journal.pcbi.1010199 |
| _version_ | 1811209174287122432 |
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| author | Mikahl Banwarth-Kuhn Kevin Rodriguez Christian Michael Calvin-Khang Ta Alexander Plong Eric Bourgain-Chang Ali Nematbakhsh Weitao Chen Amit Roy-Chowdhury G Venugopala Reddy Mark Alber |
| author_facet | Mikahl Banwarth-Kuhn Kevin Rodriguez Christian Michael Calvin-Khang Ta Alexander Plong Eric Bourgain-Chang Ali Nematbakhsh Weitao Chen Amit Roy-Chowdhury G Venugopala Reddy Mark Alber |
| author_sort | Mikahl Banwarth-Kuhn |
| collection | DOAJ |
| description | Stem cell maintenance in multilayered shoot apical meristems (SAMs) of plants requires strict regulation of cell growth and division. Exactly how the complex milieu of chemical and mechanical signals interact in the central region of the SAM to regulate cell division plane orientation is not well understood. In this paper, simulations using a newly developed multiscale computational model are combined with experimental studies to suggest and test three hypothesized mechanisms for the regulation of cell division plane orientation and the direction of anisotropic cell expansion in the corpus. Simulations predict that in the Apical corpus, WUSCHEL and cytokinin regulate the direction of anisotropic cell expansion, and cells divide according to tensile stress on the cell wall. In the Basal corpus, model simulations suggest dual roles for WUSCHEL and cytokinin in regulating both the direction of anisotropic cell expansion and cell division plane orientation. Simulation results are followed by a detailed analysis of changes in cell characteristics upon manipulation of WUSCHEL and cytokinin in experiments that support model predictions. Moreover, simulations predict that this layer-specific mechanism maintains both the experimentally observed shape and structure of the SAM as well as the distribution of WUSCHEL in the tissue. This provides an additional link between the roles of WUSCHEL, cytokinin, and mechanical stress in regulating SAM growth and proper stem cell maintenance in the SAM. |
| first_indexed | 2024-04-12T04:33:56Z |
| format | Article |
| id | doaj.art-d469c940192541b38523b08fbd564495 |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2024-04-12T04:33:56Z |
| publishDate | 2022-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-d469c940192541b38523b08fbd5644952022-12-22T03:47:51ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582022-06-01186e101019910.1371/journal.pcbi.1010199Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance.Mikahl Banwarth-KuhnKevin RodriguezChristian MichaelCalvin-Khang TaAlexander PlongEric Bourgain-ChangAli NematbakhshWeitao ChenAmit Roy-ChowdhuryG Venugopala ReddyMark AlberStem cell maintenance in multilayered shoot apical meristems (SAMs) of plants requires strict regulation of cell growth and division. Exactly how the complex milieu of chemical and mechanical signals interact in the central region of the SAM to regulate cell division plane orientation is not well understood. In this paper, simulations using a newly developed multiscale computational model are combined with experimental studies to suggest and test three hypothesized mechanisms for the regulation of cell division plane orientation and the direction of anisotropic cell expansion in the corpus. Simulations predict that in the Apical corpus, WUSCHEL and cytokinin regulate the direction of anisotropic cell expansion, and cells divide according to tensile stress on the cell wall. In the Basal corpus, model simulations suggest dual roles for WUSCHEL and cytokinin in regulating both the direction of anisotropic cell expansion and cell division plane orientation. Simulation results are followed by a detailed analysis of changes in cell characteristics upon manipulation of WUSCHEL and cytokinin in experiments that support model predictions. Moreover, simulations predict that this layer-specific mechanism maintains both the experimentally observed shape and structure of the SAM as well as the distribution of WUSCHEL in the tissue. This provides an additional link between the roles of WUSCHEL, cytokinin, and mechanical stress in regulating SAM growth and proper stem cell maintenance in the SAM.https://doi.org/10.1371/journal.pcbi.1010199 |
| spellingShingle | Mikahl Banwarth-Kuhn Kevin Rodriguez Christian Michael Calvin-Khang Ta Alexander Plong Eric Bourgain-Chang Ali Nematbakhsh Weitao Chen Amit Roy-Chowdhury G Venugopala Reddy Mark Alber Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance. PLoS Computational Biology |
| title | Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance. |
| title_full | Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance. |
| title_fullStr | Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance. |
| title_full_unstemmed | Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance. |
| title_short | Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance. |
| title_sort | combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance |
| url | https://doi.org/10.1371/journal.pcbi.1010199 |
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