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 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.
Institute of Biotechnology, University of Helsinki, Helsinki, Finland; Computational and Systems Biology, John Innes Centre, Norwich United Kingdom; Department of Biosciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, Finland.
Sedeer
S
el-Showk
Institute of Biotechnology, University of Helsinki, Helsinki, Finland; Department of Biosciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, Finland.
Hanna
H
Help-Rinta-Rahko
Institute of Biotechnology, University of Helsinki, Helsinki, Finland; Department of Biosciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, Finland.
Tiina
T
Blomster
Institute of Biotechnology, University of Helsinki, Helsinki, Finland; Department of Biosciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, Finland.
Riccardo
R
Siligato
Computational and Systems Biology, John Innes Centre, Norwich United Kingdom.
Athanasius F M
AF
Marée
Institute of Biotechnology, University of Helsinki, Helsinki, Finland; Department of Biosciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, Finland.
Ari Pekka
AP
Mähönen
Computational and Systems Biology, John Innes Centre, Norwich United Kingdom.
Verônica A
VA
Grieneisen
D017360:Arabidopsis / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000378:metabolism; D003198:Computer Simulation; D003583:Cytokinins / Q000378:metabolism*; D007210:Indoleacetic Acids / Q000378:metabolism*; D026901:Membrane Transport Proteins; D008954:Models, Biological; D010937:Plant Growth Regulators / Q000378:metabolism; D018517:Plant Roots / Q000254:growth & development*; D058526:Plant Vascular Bundle / Q000254:growth & development*
D029681:Arabidopsis Proteins; D003583:Cytokinins; D007210:Indoleacetic Acids; D026901:Membrane Transport Proteins; D010937:Plant Growth Regulators