Rapid and reversible root growth inhibition by TIR1 auxin signalling

Abstract

The phytohormone auxin is the information carrier in a plethora of developmental and physiological processes in plants. It has been firmly established that canonical, nuclear auxin signalling acts through regulation of gene transcription. Here, we combined microfluidics, live imaging, genetic engineering and computational modelling to reanalyse the classical case of root growth inhibition by auxin. We show that Arabidopsis roots react to addition and removal of auxin by extremely rapid adaptation of growth rate. This process requires intracellular auxin perception but not transcriptional reprogramming. The formation of the canonical TIR1/AFB-Aux/IAA co-receptor complex is required for the growth regulation, hinting to a novel, non-transcriptional branch of this signalling pathway. Our results challenge the current understanding of root growth regulation by auxin and suggest another, presumably non-transcriptional, signalling output of the canonical auxin pathway.

Auxin‐induced actin cytoskeleton rearrangements require AUX1

“…S6; Table S7). Increased filament density appeared before strong changes in angle and parallelness; the 30 s timeframe of IAA-induced root growth inhibition reported in Fendrych et al (2018) is much faster than gross actin reorganization was discernable, at least by current methods. Still, these are the first data that quantitatively document actin's short-term response to moderate doses of IAA, showing that actin becomes more 'organized' in response to a treatment that inhibits growth.…”

“…In order to decipher which actin parameter(s) coincided with cell expansion, and find stronger indicators of causality, we treated roots with the natural auxin IAA, which inhibits root growth within minutes (Hejnowicz & Erickson, 1968;Fendrych et al, 2018). Auxin affects actin organization and dynamics, and inhibits root growth (reviewed in Zhu & Geisler, 2015;Fendrych et al, 2018), known to depend on an intact cytoskeleton (reviewed in Hussey et al, 2006, andLi et al, 2015a). Yet, actin response following short-term auxin treatmentsthat is, a direct linkremains undetermined.…”

“…New Phytologist Erickson, 1968;Band et al, 2012;Fendrych et al, 2018), decreased extent of overall filament bundling and induced increased density, longitudinality, and parallelness within 20-30 min. That the cytoskeleton looks 'organized'more longitudinal and parallelin response to IAA, which inhibits growth within minutes (Hejnowicz & Erickson, 1968;Fendrych et al, 2018), definitively demonstrates that increased 'organization' does not inherently contribute to expansion.…”

“…New Phytologist Erickson, 1968;Band et al, 2012;Fendrych et al, 2018), decreased extent of overall filament bundling and induced increased density, longitudinality, and parallelness within 20-30 min. That the cytoskeleton looks 'organized'more longitudinal and parallelin response to IAA, which inhibits growth within minutes (Hejnowicz & Erickson, 1968;Fendrych et al, 2018), definitively demonstrates that increased 'organization' does not inherently contribute to expansion. By showing that as cell lengths and elongation rates increase, so too does extent of actin bundling (Figs 1, S1, S3), we have disproven the hypothesis that bundles inhibit expansion (Gilliland et al, 2003;Holweg et al, 2004;Rahman et al, 2007).…”

Relative Contribution of PIN-Containing Secretory Vesicles and Plasma Membrane PINs to the Directed Auxin Transport: Theoretical Estimation

“…Nevertheless, we have to check, that vesicles will contain at least one molecule. In the volume of a vesicle (maximum 2.7 × 10 5 nm 3 ) there will be initially $N_v^{t=0}=A_c\cdot V_v=0.005$ molecules if cytoplasmic auxin concentration $A_c=30 \mathrm{nM}$, which is a plausible estimate for the root epidermis [29]. For the lowest possible accumulation ratio $R=2800$, the number of molecules in one vesicle will be:$N_v=A_c\cdot V_v·R\approx \mathrm{bold14},$ which is a minimal requirement for vesicular transport.…”