Plant growth and architecture is regulated by the polar distribution of the hormone auxin. Polarity and flexibility of this process is provided by constant cycling of auxin transporter vesicles along actin filaments, coordinated by a positive auxin-actin feedback loop. Both polar auxin transport and vesicle cycling are inhibited by synthetic auxin transport inhibitors, such as 1-N-naphthylphthalamic acid (NPA), counteracting the effect of auxin; however, underlying targets and mechanisms are unclear. Using NMR, we map the NPA binding surface on the Arabidopsis thaliana ABCB chaperone TWISTED DWARF1 (TWD1). We identify ACTIN7 as a relevant, although likely indirect, TWD1 interactor, and show TWD1-dependent regulation of actin filament organization and dynamics and that TWD1 is required for NPA-mediated actin cytoskeleton remodeling. The TWD1-ACTIN7 axis controls plasma membrane presence of efflux transporters, and as a consequence act7 and twd1 share developmental and physiological phenotypes indicative of defects in auxin transport. These can be phenocopied by NPA treatment or by chemical actin (de)stabilization. We provide evidence that TWD1 determines downstream locations of auxin efflux transporters by adjusting actin filament debundling and dynamizing processes and mediating NPA action on the latter. This function appears to be evolutionary conserved since TWD1 expression in budding yeast alters actin polarization and cell polarity and provides NPA sensitivity.

CEITEC Central European Institute of Technology Masaryk University CZ 625 00 Brno Czech Republic

Centro de Biotecnología y Genómica de Plantas 28223 Pozuelo de Alarcón Madrid Spain

Cytoskeleton and Cancer Progression Laboratory of Experimental Cancer Research Department of Oncology Luxembourg Institute of Health L 1526 Luxembourg Luxembourg

Department of Biology University of Fribourg CH 1700 Fribourg Switzerland

Department of Biology University of Fribourg CH 1700 Fribourg Switzerland Department of Plant and Microbial Biology University of Zurich CH 8008 Zurich Switzerland

Department of Biology University of Fribourg CH 1700 Fribourg Switzerland Institute of Evolutionary Biology and Environmental Studies University of Zurich CH 8057 Zurich Switzerland

Department of Plant and Microbial Biology University of Zurich CH 8008 Zurich Switzerland

Institute of Cell Dynamics and Imaging University of Münster D 48149 Münster Germany

Institute of Complex Systems ICS 6 Structural Biochemistry D 52425 Jülich Germany

Institute of Science and Technology Austria A 3400 Klosterneuburg Austria

LINV DIPSAA Università di Firenze 50019 Florence Italy

Max Planck Research Unit for Enzymology of Protein Folding D 06099 Halle Germany

Max Planck Research Unit for Enzymology of Protein Folding D 06099 Halle Germany Department of Enzymology Martin Luther University Halle Wittenberg Institute of Biochemistry and Biotechnology D 06099 Halle Germany

Max Planck Research Unit for Enzymology of Protein Folding D 06099 Halle School of Pharmacy and Biochemistry University of Buenos Aires C1113AAD Buenos Aires Argentina

Plant Global Educational Project Graduate School of Biological Sciences Nara Institute of Science and Technology Ikoma 630 0192 Japan

University of Bonn Mulliken Center for Theoretical Chemistry Institute for Physical and Theoretical Chemistry D 53115 Bonn Germany

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