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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 plants1. It has been firmly established that canonical, nuclear auxin signalling acts through regulation of gene transcription2. Here, we combined microfluidics, live imaging, genetic engineering and computational modelling to reanalyse the classical case of root growth inhibition3 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.

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Fig. 1: Nanomolar concentrations of auxin reversibly inhibit root growth.
Fig. 2: Roots rapidly adapt growth rate to auxin application and removal.
Fig. 3: Rapid root growth inhibition depends on auxin levels inside the cell.
Fig. 4: Root growth inhibition requires the TIR1/AFB–Aux/IAA auxin co-receptor.

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Acknowledgements

The authors thank R. Hauschild for help with image analysis. M.F. was supported by the Austrian Science Fund (FWF) (M 2128-B21), and in the final stages of the project by the Czech Science Foundation (18-10116Y). M.A. was supported by the Austrian Science Fund (FWF) (M2379-B28). Additional funding for M.G. was received from the Ministry of Education of the Czech Republic/MŠMT project NPUI-LO1417. N.U. received MEXT/JSPS KAKENHI JP16H01462, S.H. received JP17H06350, K.T. received JP26440140 and K.U.T. received JP16H01237. K.U.T. is supported by GBMF Grant No. 3035. S.H. is a JST PRESTO Investigator and K.U.T. is an HHMI-GBMF Investigator. J.F. acknowledges the ERC Advanced Grants (ETAP).

Author information

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Authors

Contributions

M.F. initiated the project, acquired funding, performed the experiments, analysed the data and wrote the manuscript. M.A. created the computational model of auxin fluxes and wrote the manuscript. J.M. designed, optimized and fabricated the microfluidic devices. M.G. performed experiments and edited the manuscript. S.H., K.T., N.U. and K.U.T. designed, synthesized and developed the engineered cvxIAA–ccvTIR1 system and edited the manuscript. J.F. initiated the project, acquired funding and wrote the manuscript.

Corresponding author

Correspondence to Jiří Friml.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Text, Supplementary Figures 1–5, Supplementary Tables 1–4 and Supplementary References

Reporting Summary

Supplementary Data 1

Contains data supporting the results in the paper

Supplementary Video 1

The reaction of a root to addition and removal of 10 nM IAA. This movie is a spectacular demonstration of the transient nature of the root growth inhibition by auxin. The root almost instantaneously limits growth when IAA is added (marked by the magenta dye), and the growth is resumed following IAA removal

Supplementary Video 2

aux1 mutant compared to control after addition of 5 nM IAA auxin (indicated by OFF and ON)

Supplementary Video 3

Modelled temporal dynamics of IAA intracellular accumulation in control and aux1 modelled roots

Supplementary Video 4

The reaction of ccvTIR1 and controlTIR1 roots to the addition and removal of 50 nM cvxIAA (false coloured in blue)

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Fendrych, M., Akhmanova, M., Merrin, J. et al. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nature Plants 4, 453–459 (2018). https://doi.org/10.1038/s41477-018-0190-1

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