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ABSTRACT The prominent and evolutionarily ancient role of the plant hormone auxin is the regulation of cell expansion1. Cell expansion requires ordered arrangement of the cytoskeleton2 but

molecular mechanisms underlying its regulation by signalling molecules including auxin are unknown. Here we show in the model plant _Arabidopsis thaliana_ that in elongating cells exogenous

application of auxin or redistribution of endogenous auxin induces very rapid microtubule re-orientation from transverse to longitudinal, coherent with the inhibition of cell expansion. This

fast auxin effect requires auxin binding protein 1 (ABP1) and involves a contribution of downstream signalling components such as ROP6 GTPase, ROP-interactive protein RIC1 and the

microtubule-severing protein katanin. These components are required for rapid auxin- and ABP1-mediated re-orientation of microtubules to regulate cell elongation in roots and dark-grown

hypocotyls as well as asymmetric growth during gravitropic responses. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution

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about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS ABP1–TMK AUXIN PERCEPTION FOR GLOBAL PHOSPHORYLATION AND AUXIN

CANALIZATION Article 07 September 2022 MECHANISMS OF AUXIN ACTION IN PLANT GROWTH AND DEVELOPMENT Article 19 May 2025 REGULATION OF AUXIN RESPONSE FACTOR CONDENSATION AND NUCLEO-CYTOPLASMIC

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(1999) Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS We thank R. Dixit for performing complementary experiments, D. W. Ehrhardt and T. Hashimoto for providing the seeds

of TUB6–RFP and EB1b–GFP respectively, E. Zazimalova, J. Petrasek and M. Fendrych for discussing the manuscript and J. Leung for text optimization. This work was supported by the European

Research Council (project ERC-2011-StG-20101109-PSDP, to J.F.), ANR blanc AuxiWall project (ANR-11-BSV5-0007, to C.P.-R. and L.G.) and the Agency for Innovation by Science and Technology

(IWT) (to H.R.). This work benefited from the facilities and expertise of the Imagif Cell Biology platform (http://www.imagif.cnrs.fr), which is supported by the Conseil Général de

l’Essonne. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria, Xu Chen, Hongjiang Li, Robert

Hauschild, Hana Rakusová, Eva Benkova & Jiří Friml * Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie (VIB), Ghent University, B-9052 Gent, Belgium, Xu Chen, 

Hongjiang Li, Anas Abuzeineh, Hana Rakusová, Eva Benkova & Jiří Friml * Department of Plant Biotechnology and Genetics, Ghent University, B-9052 Gent, Belgium, Xu Chen, Hongjiang Li, 

Anas Abuzeineh, Hana Rakusová, Eva Benkova & Jiří Friml * Institut des Sciences du Végétal, UPR2355 CNRS, Saclay Plant Sciences LabEx, 1 Avenue de la Terrasse, 91198 Gif sur Yvette,

Cedex, France, Laurie Grandont, Sébastien Paque & Catherine Perrot-Rechenmann Authors * Xu Chen View author publications You can also search for this author inPubMed Google Scholar *

Laurie Grandont View author publications You can also search for this author inPubMed Google Scholar * Hongjiang Li View author publications You can also search for this author inPubMed 

Google Scholar * Robert Hauschild View author publications You can also search for this author inPubMed Google Scholar * Sébastien Paque View author publications You can also search for this

author inPubMed Google Scholar * Anas Abuzeineh View author publications You can also search for this author inPubMed Google Scholar * Hana Rakusová View author publications You can also

search for this author inPubMed Google Scholar * Eva Benkova View author publications You can also search for this author inPubMed Google Scholar * Catherine Perrot-Rechenmann View author

publications You can also search for this author inPubMed Google Scholar * Jiří Friml View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS X.C.,

L.G., C.P.-R. and J.F. conceived the study and designed experiments. X.C. performed experiments in roots, and L.G. performed experiments in hypocotyls. H.L., S.P. and A.A. assisted in

microscopy and data generation. H.R. generated partial double mutants. R.H. did bioinformatics analysis. E.B. helped with discussion of the data. X.C., L.G., C.P.-R. and J.F. wrote the

manuscript. CORRESPONDING AUTHORS Correspondence to Catherine Perrot-Rechenmann or Jiří Friml. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests.

EXTENDED DATA FIGURES AND TABLES EXTENDED DATA FIGURE 1 AUXIN INDUCES MICROTUBULE REARRANGEMENT IN ROOT CELLS. A, Schematic diagram of root and dark-grown hypocotyl growth. The growth

direction of the root and hypocotyl is named as the cell growth axis. The observed cells for microtubules array were in the transition zone (highlighted by red line) of roots and in the

elongation zone of dark-grown hypocotyls (highlighted by grey frame). The arrays of microtubules in root and hypocotyl were depicted for the expanding cells. B–F, MAP4–GFP or TUA6–RFP

visualization of microtubule orientation in roots was performed by time-lapse observation (every 10 min; prime (′), minutes) following 100 nM NAA or IAA treatment, and deviated angles of

individual microtubules were quantified as transverse microtubules (90 ± 30°) or longitudinal microtubules (0–60°/120–180°). In C and F, Student’s _t_-test was calculated for transverse

microtubules compared with untreated roots (*_P_ < 0.05; **_P_ < 0.001). G, H, MAP4–GFP visualization and quantification of microtubule orientation in roots after 1 µM 2-NAA treatment

for 60 min or after transfer of seedlings on acidified 1/2 Murashige and Skoog medium at pH 4.9 for 30, 90 and 180 minutes. Student’s _t_-test was calculated for transverse microtubules in

treated samples compared with 1/2 Murashige and Skoog medium (pH 5.8) growing roots used as controls (**_P_ < 0.001). I–K, Auxin distribution approximated by DII-VENUS at the lower side

(LS) and upper side (US) of 90° re-oriented WT root (in DII-VENUS background). Enlarged pictures (I) are shown as the frames highlighted (K). Signal intensity is represented by the colour

code as indicated. The relative signal for the upper side and lower side (J) is expressed compared with the signal in the respective frame before gravistimulation. Student’s _t_-test was

calculated for the signal between the upper and lower sides at each time point (**_P_ < 0.001). In all panels, average values are shown and error bars are s.e.m. Scale bars, 5 μm (B, D,

E, G) and 30 μm (K). EXTENDED DATA FIGURE 2 FUNCTIONAL INACTIVATION OF ABP1 RESULTS IN MICROTUBULE DEFECTS GRADUALLY INCREASING WITH TIME OF ABP1 INACTIVATION. A, B, MAP4–GFP visualization

of microtubule orientation in WT and _tir1-1 afb1-1 afb2-1 afb3-1_ (abbreviated as _tir1afb1,2,3_) seedlings following 100 nM NAA treatment for 60 min. The proportion of cells with the four

categories of microtubule orientation patterns was determined, and Student’s _t_-test was calculated for the category of transverse microtubule compared with WT treated in the same condition

(**_P_ < 0.001). C–F, MAP4–GFP visualization and quantification of microtubule orientation in roots (C, D) or dark-grown hypocotyls (E, F) of WT, SS12S and SS12K seedlings following

different times of ethanol induction as indicated. Student’s _t_-test was calculated for the transverse microtubules compared with WT exposed for the same time to ethanol vapours as the

conditional ABP1 lines (*_P_ < 0.05, **_P_ < 0.001). In all panels, average values are shown and error bars are s.e.m. Scale bars, 5 μm (A, C) and 10 μm (E). EXTENDED DATA FIGURE 3

ABP1 IS INVOLVED IN MICROTUBULE REARRANGEMENT FOLLOWING GRAVISTIMULATION. A, Rearrangement of microtubules at the lower side compared with the upper side of 90° re-oriented roots of WT,

SS12S, SS12K and _abp1-5_ (all expressing MAP4–GFP). Two different types of microtubule orientation (90 ± 30° or 0–60°/120–180°) were quantified. Student’s _t_-test was calculated for the

category of transverse microtubules compared with each 0′ time point and calculated for transverse microtubules in the lower side compared with the upper side at each time point (**_P_ < 

0.001). B, C, Auxin distribution simulated by DII-VENUS at the lower side compared with the upper side of 90° re-oriented roots of SS12S and SS12K (all in DII-VENUS background; enlarged

pictures were visualized in the frames highlighted). Image stacks were taken every 10 minutes, in total for 60 minutes. The ratio of the lower side signal divided by that of the upper side

is shown in the chart (C). Student’s _t_-test was calculated for the signal ratio at each time point of SS12S/K compared with WT (**_P_ < 0.001). Signal intensity is represented by the

colour code as indicated. Data for SS12S and SS12K (B) are compared with WT (Extended Data Fig. 1i–k). D, The deviated angles of 90° gravistimulated-roots of WT, _abp1-5_, SS12S and SS12K

seedlings were calculated every 30 min, in total for 8 h (Student’s _t_-test, *_P_ < 0.05, **_P_ < 0.001). In all panels, average values are shown and error bars are s.e.m. Scale bars,

5 μm (A) and 30 μm (B). EXTENDED DATA FIGURE 4 THE EFFECT OF AUXIN ON FAST RESPONSIVENESS OF MICROTUBULE DYNAMICS IS DEPENDENT ON ABP1. A, B, Acquisition and quantification of the rate of

EB1b movement in roots of untreated or 100 nM NAA-treated (60 min) WT or SS12K (expressing EB1b–GFP) by measuring EB1b–GFP growth events as highlighted by red lines (Student’s _t_-test, _P_ 

> 0.05). Box plots indicate the 25th centile (bottom boundary), median (middle line), 75th centile (top boundary), the nearest observations within 1.5 times, the interquartile range and

outliers. C, EB1b movement was simulated as transverse (blue, 90 ± 30°) or longitudinal (red, 0–60°/120–180°) trajectories before (0′) and after (180′′) 100 nM NAA treatment in WT background

(colour maps). The blue/red surface ratio is quantified on the chart (_n_ = 5); C corresponds to Fig. 3a. D, Microtubule orientation patterns after 400 µM cordycepin plus NAA co-treatment.

Student’s _t_-test was calculated for the category of transverse microtubule compared with only cordycepin treatment (**_P_ < 0.001). E, EB1b trajectories (simulated by time-stack from 10

 min videos) were visualized and quantified after DMSO, IAA (1 µM), PEO-IAA (10 µM) and PEO-IAA (10 µM) plus IAA (1 µM) treatments. The left panel shows successive frames of 90′ acquisitions

following IAA application of pre-treated PEO-IAA WT roots. Student’s _t_-test was calculated for the category of transverse microtubules compared with DMSO treatment at each time point

(**_P_ < 0.001). F–I, Projections of EB1b–GFP in SS12K roots (F) and quantification (G) from every 15 s acquisition during 10 min (Supplementary Videos 4 and 6) following DMSO or 100 nM

NAA application (_n_ = 10). Blue and red strips represent transverse (90 ± 30°) and oblique/longitudinal (0–60°/120–180°) directions, respectively (F). Colour maps show the simulated

transverse or longitudinal trajectories of EB1b before (0′) and after (180′′) 100 nM NAA treatment in SS12K (H) or SS12S (I) roots. The blue/red surface ratio is quantified on the charts

(_n_ = 5) (H, I). The data of SS12S (I) correspond to Fig. 3b, and the data of SS12S and SS12K (F–I) are compared with WT (Fig. 3a and Extended Data Fig. 4c). In all panels except B, average

values are shown, error bars are s.e.m. and scale bars are 5 μm. EXTENDED DATA FIGURE 5 OVEREXPRESSED ABP1-INDUCED EFFECT OF AUXIN ON FAST RESPONSIVENESS OF MICROTUBULE DYNAMICS. A–C, ABP1

and ABP1–GFP transcripts (A) and ABP1 protein level (B, C) were detected in WT and XVE ≫ ABP1-OE line before and after 2 µM oestradiol induction for 12 h or 48 h before RNA or protein

extraction. The transcript levels of ABP1 in WT with DMSO treatment were standardized as ‘1’ (A). The 22 kDa native ABP1 band and 49KDa ABP1–GFP band were detected and quantified in the

right chart. The protein level of native ABP1 or ABP1–GFP in WT was standardized as ‘1’ for each ABP1 and ABP1–GFP, respectively (B, C). Student’s _t_-test, **_P_ < 0.001. D, Time-lapse

observation of microtubule orientation in the roots of XVE ≫ ABP1-OE roots expressing TUA6–RFP, WT and _abp1-5_ (both expressing MAP4–GFP) upon 100 nM NAA treatment. The percentage of

re-oriented microtubules (0–60°/120–180°) was quantified. Re-oriented microtubules in the inducible XVE ≫ ABP1-OE TUA6–RFP roots were calculated compared with none-inducible roots, and

_abp1-5_ MAP4–GFP was compared with MAP4–GFP at each time point (Student’s _t_-test, *_P_ < 0.05, **_P_ < 0.001). In all panels, average values are shown, error bars are s.e.m and

scale bars are 5 μm. EXTENDED DATA FIGURE 6 CALCIUM STARVATION DISRUPTS MICROTUBULE ORIENTATION AND HIGH CALCIUM INCREASES MICROTUBULE DEPOLYMERIZATION. Orientation and polymerization

statuses of microtubules were visualized following transfer of seedlings to different concentrations of CaCl2 for 30, 90 or 180 min. Low calcium levels disrupted microtubule organization,

leading to a predominantly random pattern; high calcium caused microtubule depolymerization. Student’s _t_-test was calculated for the category of transverse microtubules compared with

seedlings grown and transferred on standard 1/2 Murashige and Skoog medium (with 1.5 mM CaCl2) (*_P_ < 0.05, **_P_ < 0.001). In all panels, average values are shown, error bars are

s.e.m. and scale bars are 5 μm. EXTENDED DATA FIGURE 7 AUXIN–ABP1 CONTROLS MICROTUBULE ARRANGEMENT THROUGH DOWNSTREAM ROP6–RIC1–KTN1 SIGNALLING. A, MAP4–GFP visualization of microtubule

orientation in the root of WT, _rop6-1_, _ric1-1_, SS12S _ric1-1_ and SS12K _ric1-1_ following DMSO application for 60 min. Pictures in A correspond to quantifications in Fig. 4a. B, C,

Microtubule re-orientation patterns were visualized by MAP4–GFP in the roots of WT and _rop6-1_+/− following DMSO or 100 nM NAA application for 60 min (Student’s _t_-test, _P_ > 0.05). D,

Transcript level of the _scFv12_ coding the recombinant antibody responsible for ABP1 knockdown in WT, _ric1-1_, _ktn1_, SS12S, SS12K, SS12S _ric1-1_, SS12K _ric1-1_, SS12S _ktn1_ and SS12K

_ktn1_ after 48 h ethanol induction. The transcript level of the _scFv12_ in SS12S was standardized as ‘1’ (Student’s _t_-test, _P_ > 0.05). E, Microtubule orientation by MAP4–GFP in

dark-grown hypocotyls of WT, SS12K, _ktn1_ and SS12K _ktn1_ (with 24 h ethanol induction) following DMSO application for 60 min. Pictures in e correspond to Fig. 4b. In all panels, average

values are shown and error bars are s.e.m. Scale bars, 5 μm (A, B) and 10 μm (E). SUPPLEMENTARY INFORMATION THE TRAJECTORIES OF EB1B IN WT BACKGROUND FOLLOWING DMSO TREATMENT EB1b-GFP

seedlings were mounted on DMSO-contained 1/2 MS glass slides and imaged immediately for 10min. EB1b-GFP comets illustrate major transversal MT growth trajectories (90±30°). Corresponding to

Fig. 3a. (MOV 3725 kb) THE TRAJECTORIES OF EB1B IN WT BACKGROUND FOLLOWING 100NM NAA TREATMENT EB1b-GFP seedlings were mounted on 1/2 MS glass slides containing 100nM NAA and imaged

immediately for 10min. EB1b-GFP moves mainly along 90±30° transversal direction in the beginning (0-60sec), while increasing EB1b tracks switch along oblique/longitudinal direction

(0-60°/120-180°) after 75sec. Corresponding to Fig. 3a. (MOV 2184 kb) THE TRAJECTORIES OF EB1B IN ABP1 KNOCKDOWN LINES FOLLOWING DMSO TREATMENT 48h ethanol induced SS12S or SS12K seedlings

expressing EB1b-GFP were mounted on DMSO-contained 1/2 MS glass slides and imaged immediately for 10min. High proportion of EB1b-GFP moves in oblique/longitudinal directions. Corresponding

to Fig. 3b, Extended Data Fig. 4d. (MOV 1813 kb) THE TRAJECTORIES OF EB1B IN ABP1 KNOCKDOWN LINES FOLLOWING DMSO TREATMENT 48h ethanol induced SS12S or SS12K seedlings expressing EB1b-GFP

were mounted on DMSO-contained 1/2 MS glass slides and imaged immediately for 10min. High proportion of EB1b-GFP moves in oblique/longitudinal directions. Corresponding to Fig. 3b, Extended

Data Fig. 4d. (MOV 1383 kb) THE TRAJECTORIES OF EB1B IN SS12S OR SS12K BACKGROUND FOLLOWING 100NM NAA TREATMENT 48h ethanol induced SS12S or SS12K seedlings expressing EB1b-GFP were mounted

on 1/2 MS glass slides containing 100nM NAA and imaged immediately for 10min. Compared with WT, no consistent switch of EB1b trajectories to longitudinal directions but only few stochastic

changes were observed. Corresponding to Fig. 3b, Extended Data Fig. 4d. (MOV 1717 kb) THE TRAJECTORIES OF EB1B IN SS12S OR SS12K BACKGROUND FOLLOWING 100NM NAA TREATMENT 48h ethanol induced

SS12S or SS12K seedlings expressing EB1b-GFP were mounted on 1/2 MS glass slides containing 100nM NAA and imaged immediately for 10min. Compared with WT, no consistent switch of EB1b

trajectories to longitudinal directions but only few stochastic changes were observed. Corresponding to Fig. 3b, Extended Data Fig. 4d. (MOV 2100 kb) POWERPOINT SLIDES POWERPOINT SLIDE FOR

FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3 POWERPOINT SLIDE FOR FIG. 4 RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Chen, X.,

Grandont, L., Li, H. _et al._ Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules. _Nature_ 516, 90–93 (2014). https://doi.org/10.1038/nature13889 Download

citation * Received: 12 November 2013 * Accepted: 23 September 2014 * Published: 17 November 2014 * Issue Date: 04 December 2014 * DOI: https://doi.org/10.1038/nature13889 SHARE THIS ARTICLE

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