Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out.
An auxin maximum is positioned along the xylem axis of the Arabidopsis root tip. The pattern depends on mutual feedback between auxin and cytokinins mediated by the PIN class of auxin efflux transporters and AHP6, an inhibitor of cytokinin signalling. This interaction has been proposed to regulate t...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2015-10-01
|
| Series: | PLoS Computational Biology |
| Online Access: | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004450&type=printable |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849331163775107072 |
|---|---|
| author | Sedeer el-Showk Hanna Help-Rinta-Rahko Tiina Blomster Riccardo Siligato Athanasius F M Marée Ari Pekka Mähönen Verônica A Grieneisen |
| author_facet | Sedeer el-Showk Hanna Help-Rinta-Rahko Tiina Blomster Riccardo Siligato Athanasius F M Marée Ari Pekka Mähönen Verônica A Grieneisen |
| author_sort | Sedeer el-Showk |
| collection | DOAJ |
| description | An auxin maximum is positioned along the xylem axis of the Arabidopsis root tip. The pattern depends on mutual feedback between auxin and cytokinins mediated by the PIN class of auxin efflux transporters and AHP6, an inhibitor of cytokinin signalling. This interaction has been proposed to regulate the size and the position of the hormones' respective signalling domains and specify distinct boundaries between them. To understand the dynamics of this regulatory network, we implemented a parsimonious computational model of auxin transport that considers hormonal regulation of the auxin transporters within a spatial context, explicitly taking into account cell shape and polarity and the presence of cell walls. Our analysis reveals that an informative spatial pattern in cytokinin levels generated by diffusion is a theoretically unlikely scenario. Furthermore, our model shows that such a pattern is not required for correct and robust auxin patterning. Instead, auxin-dependent modifications of cytokinin response, rather than variations in cytokinin levels, allow for the necessary feedbacks, which can amplify and stabilise the auxin maximum. Our simulations demonstrate the importance of hormonal regulation of auxin efflux for pattern robustness. While involvement of the PIN proteins in vascular patterning is well established, we predict and experimentally verify a role of AUX1 and LAX1/2 auxin influx transporters in this process. Furthermore, we show that polar localisation of PIN1 generates an auxin flux circuit that not only stabilises the accumulation of auxin within the xylem axis, but also provides a mechanism for auxin to accumulate specifically in the xylem-pole pericycle cells, an important early step in lateral root initiation. The model also revealed that pericycle cells on opposite xylem poles compete for auxin accumulation, consistent with the observation that lateral roots are not initiated opposite to each other. |
| format | Article |
| id | doaj-art-95cb548b82fd4fb78b15a8e85b987906 |
| institution | Kabale University |
| issn | 1553-734X 1553-7358 |
| language | English |
| publishDate | 2015-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj-art-95cb548b82fd4fb78b15a8e85b9879062025-08-20T03:46:42ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582015-10-011110e100445010.1371/journal.pcbi.1004450Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out.Sedeer el-ShowkHanna Help-Rinta-RahkoTiina BlomsterRiccardo SiligatoAthanasius F M MaréeAri Pekka MähönenVerônica A GrieneisenAn auxin maximum is positioned along the xylem axis of the Arabidopsis root tip. The pattern depends on mutual feedback between auxin and cytokinins mediated by the PIN class of auxin efflux transporters and AHP6, an inhibitor of cytokinin signalling. This interaction has been proposed to regulate the size and the position of the hormones' respective signalling domains and specify distinct boundaries between them. To understand the dynamics of this regulatory network, we implemented a parsimonious computational model of auxin transport that considers hormonal regulation of the auxin transporters within a spatial context, explicitly taking into account cell shape and polarity and the presence of cell walls. Our analysis reveals that an informative spatial pattern in cytokinin levels generated by diffusion is a theoretically unlikely scenario. Furthermore, our model shows that such a pattern is not required for correct and robust auxin patterning. Instead, auxin-dependent modifications of cytokinin response, rather than variations in cytokinin levels, allow for the necessary feedbacks, which can amplify and stabilise the auxin maximum. Our simulations demonstrate the importance of hormonal regulation of auxin efflux for pattern robustness. While involvement of the PIN proteins in vascular patterning is well established, we predict and experimentally verify a role of AUX1 and LAX1/2 auxin influx transporters in this process. Furthermore, we show that polar localisation of PIN1 generates an auxin flux circuit that not only stabilises the accumulation of auxin within the xylem axis, but also provides a mechanism for auxin to accumulate specifically in the xylem-pole pericycle cells, an important early step in lateral root initiation. The model also revealed that pericycle cells on opposite xylem poles compete for auxin accumulation, consistent with the observation that lateral roots are not initiated opposite to each other.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004450&type=printable |
| spellingShingle | Sedeer el-Showk Hanna Help-Rinta-Rahko Tiina Blomster Riccardo Siligato Athanasius F M Marée Ari Pekka Mähönen Verônica A Grieneisen Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out. PLoS Computational Biology |
| title | Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out. |
| title_full | Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out. |
| title_fullStr | Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out. |
| title_full_unstemmed | Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out. |
| title_short | Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out. |
| title_sort | parsimonious model of vascular patterning links transverse hormone fluxes to lateral root initiation auxin leads the way while cytokinin levels out |
| url | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004450&type=printable |
| work_keys_str_mv | AT sedeerelshowk parsimoniousmodelofvascularpatterninglinkstransversehormonefluxestolateralrootinitiationauxinleadsthewaywhilecytokininlevelsout AT hannahelprintarahko parsimoniousmodelofvascularpatterninglinkstransversehormonefluxestolateralrootinitiationauxinleadsthewaywhilecytokininlevelsout AT tiinablomster parsimoniousmodelofvascularpatterninglinkstransversehormonefluxestolateralrootinitiationauxinleadsthewaywhilecytokininlevelsout AT riccardosiligato parsimoniousmodelofvascularpatterninglinkstransversehormonefluxestolateralrootinitiationauxinleadsthewaywhilecytokininlevelsout AT athanasiusfmmaree parsimoniousmodelofvascularpatterninglinkstransversehormonefluxestolateralrootinitiationauxinleadsthewaywhilecytokininlevelsout AT aripekkamahonen parsimoniousmodelofvascularpatterninglinkstransversehormonefluxestolateralrootinitiationauxinleadsthewaywhilecytokininlevelsout AT veronicaagrieneisen parsimoniousmodelofvascularpatterninglinkstransversehormonefluxestolateralrootinitiationauxinleadsthewaywhilecytokininlevelsout |