Cytokinin acts through the auxin influx carrier AUX1 to regulate cell elongation in the root

Abstract

Hormonal interactions are crucial for plant development. In Arabidopsis, cytokinins inhibit root growth through effects on cell proliferation and cell elongation. Here, we define key mechanistic elements in a regulatory network by which cytokinin inhibits root cell elongation in concert with the hormones auxin and ethylene. The auxin importer AUX1 functions as a positive regulator of cytokinin responses in the root; mutation of AUX1 specifically affects the ability of cytokinin to inhibit cell elongation but not cell proliferation. AUX1 is required for cytokinin-dependent changes of auxin activity in the lateral root cap associated with the control of cell elongation. Cytokinin regulates root cell elongation through ethylene-dependent and -independent mechanisms, both hormonal signals converging on AUX1 as a regulatory hub. An autoregulatory circuit is identified involving the control of ARR10 and AUX1 expression by cytokinin and auxin, this circuit potentially functioning as an oscillator to integrate the effects of these two hormones. Taken together, our results uncover several regulatory circuits controlling interactions of cytokinin with auxin and ethylene, and support a model in which cytokinin regulates shootward auxin transport to control cell elongation and root growth.

A Sizer model for cell differentiation in Arabidopsis thaliana root growth

“…Together, our computational analysis predicts that the correlation between N EZ and 1/ln(r EZ ) uncovered in wild‐type data is essential to account for reduced root growth with unaltered mature cell length when the meristematic activity decreases. This prediction coincides with the decreased root growth and an unaltered mature cell length reported previously (Chaiwanon & Wang, ; Rodriguez et al , ; Street et al , ).…”

“…Moreover, modeling unveiled the relevance of the linear correlation between traits of the MZ and the EZ (i.e., 1/ln(r EZ ) and number of cells in the EZ) to drive characteristic root growth despite stochastic variability. We found this correlation essential to predict phenotypic changes in agreement with those reported in roots in which the meristematic activity is altered, but not the mature cell length (Chaiwanon & Wang, ; Rodriguez et al , ; Street et al , ). Similarly, we found it in roots treated with PAC at different concentrations, which are known to exhibit the same mature cell length, but distinct root growth (Band et al , ).…”

Lateral Root Priming Synergystically Arises from Root Growth and Auxin Transport Dynamics

“…In addition, vasculature cells tend to elongate more rootward [Campbell andTurner, 2017, Rahni andBirnbaum, 2018], thus being longer than other cell types when arriving in the TZ. Passive auxin uptake in the TZ and early EZ is further enhanced by the steep decrease in pH accompanying elongation [Barbez et al, 2017, Street et al, 2016, which causes a shift in relative importance from active to passive auxin uptake [Rutschow et al, 2014].…”

“…All normalisations were only applied for cells with a height exceeding 1.5M Zcellheight, and were not applied to lateral root cap and columella cells. Additionally, to study the influence of passive auxin uptake, rather than normalizing it for cell size, we implemented a modest pH dependent increase of background influx in the EZ [Rutschow et al, 2014,Street et al, 2016,Barbez et al, 2017. For this we implemented a tissue pH gradient, with constant high pH levels in the MZ (pH M Z = 5.8) and a steep drop of pH in the EZ (minimum pH in EZ of 4.8, reached at a distance of 150 µm from the start of the EZ), and a recovery of the same high pH levels in the DZ (reached directly at the start of the DZ).…”

“…Interestingly, it has been shown that in the TZ/EZ a significant drop in pH occurs, important for fast cell expansion. This pH drop causes a shift in the relative importance from AUX1 mediated active auxin import towards passive, background auxin influx [Rutschow et al, 2014,Street et al, 2016, Barbez et al, 2017. Therefore, rather than normalizing background influx with cell size, we investigated the importance of background influx by incorporating a modest pH dependent increase of background influx with a factor of 2.4 in the elongation zone.…”