Fluctuations in auxin levels depend upon synchronicity of cell divisions in a one-dimensional model of auxin transport

Bellows, Simon; Janes, George; Avitabile, Daniele; King, John R.; Bishopp, Anthony; Farcot, Etienne

Abstract

Auxin is a well-studied plant hormone, the spatial distribution of which remains incompletely understood. Here, we investigate the effects of cell growth and divisions on the dynamics of auxin patterning, using a combination of mathematical modelling and experimental observations. In contrast to most prior work, models are not designed or tuned with the aim to produce a specific auxin pattern. Instead, we use well-established techniques from dynamical systems theory to uncover and classify ranges of auxin patterns as exhaustively as possible as parameters are varied. Previous work using these techniques has shown how a multitude of stable auxin patterns may coexist, each attainable from a specific ensemble of initial conditions. When a key parameter spans a range of values, these steady patterns form a geometric curve with successive folds, often nicknamed a snaking diagram. As we introduce growth and cell division into a one-dimensional model of auxin distribution, we observe new behaviour which can be explained in terms of this diagram. Cell growth changes the shape of the snaking diagram, and this corresponds in turn to deformations in the patterns of auxin distribution. As divisions occur this can lead to abrupt creation or annihilation of auxin peaks. We term this phenomenon ‘snake-jumping’. Under rhythmic cell divisions, we show how this can lead to stable oscillations of auxin. We also show that this requires a high level of synchronisation between cell divisions. Using 18 hour time-lapse imaging of the auxin reporter DII:Venus in roots of Arabidopsis thaliana, we show auxin fluctuates greatly, both in terms of amplitude and periodicity, consistent with the snake-jumping events observed with non-synchronised cell divisions. Periodic signals downstream of the auxin signalling pathway have previously been recorded in plant roots. The present work shows that auxin alone is unlikely to play the role of a pacemaker in this context.

Citation

Bellows, S., Janes, G., Avitabile, D., King, J. R., Bishopp, A., & Farcot, E. (2023). Fluctuations in auxin levels depend upon synchronicity of cell divisions in a one-dimensional model of auxin transport. PLoS Computational Biology, 19(11), Article e1011646. https://doi.org/10.1371/journal.pcbi.1011646

• Journal Article Type: Article
• Acceptance Date: Nov 1, 2023
• Online Publication Date: Nov 30, 2023
• Publication Date: Nov 30, 2023
• Deposit Date: Dec 4, 2023
• Publicly Available Date: Dec 4, 2023
• Journal: PLOS Computational Biology
• Print ISSN: 1553-734X
• Electronic ISSN: 1553-7358
• Publisher: Public Library of Science
• Peer Reviewed: Peer Reviewed
• Volume: 19
• Issue: 11
• Article Number: e1011646
• DOI: https://doi.org/10.1371/journal.pcbi.1011646
• Keywords: Auxins; Cell cycle and cell division; Genetic oscillators; Meristems; Arabidopsis thaliana; Dynamical systems; Deformation; Root growth
• Public URL: https://nottingham-repository.worktribe.com/output/27874279
• Publisher URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1011646