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.

Department of Experimental Plant Biology Faculty of Science Charles University Prague Czechia

Howard Hughes Medical Institute and Department of Biology University of Washington Seattle WA USA

Institute of Science and Technology Austria Klosterneuburg Austria

Institute of Transformative Biomolecules and Graduate School of Science Nagoya University Chikusa Nagoya Japan

Komentář v

Nat Plants. 2018 Jul;4(7):410-411. doi: 10.1038/s41477-018-0196-8. PubMed

Zobrazit více v PubMed

Leyser O Auxin Signaling. Plant Physiol. 176, 465–479 (2018). PubMed PMC

Gray WM, Kepinski S, Rouse D, Leyser O & Estelle M Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001). PubMed

Evans ML, Ishikawa H & Estelle MA Responses of Arabidopsis Roots to Auxin Studied with High Temporal Resolution - Comparison of Wild-Type and Auxin-Response Mutants. Planta 194, 215–222 (1994).

Knight TA On the Direction of the Radicle and Germen during the Vegetation of Seeds. Phil. Trans. R. Soc. Lond. 96, 99–108 (1806).

Darwin C The Power of Movement in Plants. (John Murray, London, 1880).

Nemec B Ueber die art der wahrnehmung des schwek- raftreizes bei den pflanzen. Ber Dtsch Bot Ges 18, 241–245 (1900).

Adamowski M & Friml J PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27, 20–32 (2015). PubMed PMC

Went F & Thimann K Phytohormones. (1937). doi:10.1017/CBO9781107415324.004 DOI

Tan X et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640–5 (2007). PubMed

Fendrych M, Leung J & Friml J TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. Elife 5, 1–18 (2016). PubMed PMC

Uchida N et al. Chemical hijacking of auxin signaling with an engineered auxin–TIR1 pair. Nat. Chem. Biol. (2018). doi:10.1038/nchembio.2555 PubMed DOI PMC

Leyser HMO, Pickett FB, Dharmasiri S & Estelle M Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J. 10, 403–413 (1996). PubMed

Ruegger M et al. The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev. 12, 198–207 (1998). PubMed PMC

Scheitz K, Lüthen H & Schenck D Rapid auxin-induced root growth inhibition requires the TIR and AFB auxin receptors. Planta 238, 1171–1176 (2013). PubMed

Monshausen GB, Miller ND, Murphy AS & Gilroy S Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J. 65, 309–18 (2011). PubMed

Shih HW, Depew CL, Miller ND & Monshausen GB The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in arabidopsis thaliana. Curr. Biol. 25, 3119–3125 (2015). PubMed

Grossmann G et al. The RootChip: an integrated microfluidic chip for plant science. Plant Cell 23, 4234–4240 (2011). PubMed PMC

von Wangenheim D et al. Live tracking of moving samples in confocal microscopy for vertically grown roots. Elife 6, (2017). PubMed PMC

Band LRR et al. Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc. Natl. Acad. Sci. U. S. A. 109, 4668–4673 (2012). PubMed PMC

Brunoud G et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103–6 (2012). PubMed

Hoyle NP & Ish-Horowicz D Transcript processing and export kinetics are rate-limiting steps in expressing vertebrate segmentation clock genes. Proc. Natl. Acad. Sci. U. S. A. 110, E4316–24 (2013). PubMed PMC

McClure BA, Hagen G, Brown CS, Gee MA & Guilfoyle TJ Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1, 229–39 (1989). PubMed PMC

Moreno-Risueno MA et al. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329, 1306–11 (2010). PubMed PMC

MACDONALD IR & ELLIS RJ Does Cycloheximide inhibit Protein Synthesis specifically in Plant Tissues? Nature 222, 791–792 (1969).

Okushima Y et al. Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana. Plant Cell 17, 444–463 (2005). PubMed PMC

Swarup R et al. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057–1065 (2005). PubMed

Bennett MJ et al. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948–50 (1996). PubMed

Delbarre A, Muller P, Imhoff V & Guern J Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198, 532–541 (1996). PubMed

Dindas J et al. AUX1-mediated root hair auxin influx governs SCFTIR1/AFB-type Ca2+signaling. Nat. Commun. 9, 1174 (2018). PubMed PMC

Dharmasiri N et al. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109–119 (2005). PubMed

Hayashi K et al. Rational design of an auxin antagonist of the SCF(TIR1) auxin receptor complex. ACS Chem. Biol. 7, 590–8 (2012). PubMed

Swarup R et al. Structure-Function Analysis of the Presumptive Arabidopsis Auxin Permease AUX1. Plant Cell 16, 3069–3083 (2004). PubMed PMC

Grossmann G et al. Time-lapse Fluorescence Imaging of Arabidopsis Root Growth with Rapid Manipulation of The Root Environment Using The RootChip. J. Vis. Exp. e4290–e4290 (2012). doi:10.3791/4290 PubMed DOI PMC

Li L, Krens SFG, Fendrych M & Friml J Real-time Analysis of Auxin Response, Cell Wall pH and Elongation in Arabidopsis thaliana Hypocotyls. Bio-Protocol 7, 1–10 (2018). PubMed PMC

Thévenaz P, Ruttimann UE, U M, Thevenaz P, Ruttimann UE & Unser M A Pyramid Approach to Subpixel Registration Based on Intensity. IEEE Trans. Image Process. 7, 27–41 (1998). PubMed

Schneider C. a, Rasband WS & Eliceiri KW NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012). PubMed PMC

Schindelin J et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). PubMed PMC

Mapping the membrane orientation of auxin homeostasis regulators PIN5 and PIN8 in Arabidopsis thaliana root cells reveals their divergent topology

RAF-like protein kinases mediate a deeply conserved, rapid auxin response

Relative Membrane Potential Measurements Using DISBAC2(3) Fluorescence in Arabidopsis thaliana Primary Roots

The AUX1-AFB1-CNGC14 module establishes a longitudinal root surface pH profile

The AFB1 auxin receptor controls the cytoplasmic auxin response pathway in Arabidopsis thaliana

Recent insights into metabolic and signalling events of directional root growth regulation and its implications for sustainable crop production systems

The AFB1 auxin receptor controls the cytoplasmic auxin response pathway in Arabidopsis thaliana

ABP1-TMK auxin perception for global phosphorylation and auxin canalization

RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis

Expansin-mediated developmental and adaptive responses: A matter of cell wall biomechanics?

ACORBA: Automated workflow to measure Arabidopsis thaliana root tip angle dynamics

Throttling Growth Speed: Evaluation of aux1-7 Root Growth Profile by Combining D-Root system and Root Penetration Assay

Bundling up the Role of the Actin Cytoskeleton in Primary Root Growth

Auxin Metabolite Profiling in Isolated and Intact Plant Nuclei

AFB1 controls rapid auxin signalling through membrane depolarization in Arabidopsis thaliana root

Auxin Metabolome Profiling in the Arabidopsis Endoplasmic Reticulum Using an Optimised Organelle Isolation Protocol

Xyloglucan Remodeling Defines Auxin-Dependent Differential Tissue Expansion in Plants

No Time for Transcription-Rapid Auxin Responses in Plants

The TOR-Auxin Connection Upstream of Root Hair Growth

Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter