Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Auxin‐induced actin cytoskeleton rearrangements require AUX1

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.16382· OSTI ID:1599228
 [1];  [2]
  1. Department of Biological Sciences Purdue University West Lafayette IN 47907‐2064 USA, Purdue University Interdisciplinary Life Sciences Graduate Program (PULSe) Purdue University West Lafayette IN 47907 USA, Center for Plant Biology Purdue University West Lafayette IN 47907 USA
  2. Department of Biological Sciences Purdue University West Lafayette IN 47907‐2064 USA, Center for Plant Biology Purdue University West Lafayette IN 47907 USA, Department of Botany and Plant Pathology Purdue University West Lafayette IN 47907 USA
Summary

The actin cytoskeleton is required for cell expansion and implicated in cellular responses to the phytohormone auxin. However, the mechanisms that coordinate auxin signaling, cytoskeletal remodeling and cell expansion are poorly understood. Previous studies examined long‐term actin cytoskeleton responses to auxin, but plants respond to auxin within minutes. Before this work, an extracellular auxin receptor – rather than the auxin transporter AUXIN RESISTANT 1 (AUX1) – was considered to precede auxin‐induced cytoskeleton reorganization.

In order to correlate actin array organization and dynamics with degree of cell expansion, quantitative imaging tools established baseline actin organization and illuminated individual filament behaviors in root epidermal cells under control conditions and after indole‐3‐acetic acid (IAA) application. We evaluated aux1 mutant actin organization responses to IAA and the membrane‐permeable auxin 1‐naphthylacetic acid (NAA).

Cell length predicted actin organization and dynamics in control roots; short‐term IAA treatments stimulated denser and more parallel, longitudinal arrays by inducing filament unbundling within minutes. Although AUX1 is necessary for full actin rearrangements in response to auxin, cytoplasmic auxin (i.e. NAA) stimulated a lesser response.

Actin filaments became more ‘organized’ after IAA stopped elongation, refuting the hypothesis that ‘more organized’ actin arrays universally correlate with rapid growth. Short‐term actin cytoskeleton response to auxin requires AUX1 and/or cytoplasmic auxin.

Research Organization:
Purdue Univ., West Lafayette, IN (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Physical Biosciences Program
Grant/Contract Number:
FG02-04ER15526
OSTI ID:
1599228
Alternate ID(s):
OSTI ID: 1625919
OSTI ID: 1599229
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 2 Vol. 226; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (107)

Latrunculin B-Induced Plant Dwarfism: Plant Cell Elongation Is F-Actin-Dependent journal March 2001
Kinetic mechanism of end-to-end annealing of actin filaments 1 1Edited by M. F. Moody journal September 2001
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 journal April 1996
Mutants of Arabidopsis thaliana with altered responses to auxins and gravity journal December 1980
Higher extracellular pH suppresses tracheary element differentiation by affecting auxin uptake journal February 2006
Secretion marker proteins and cell-wall polysaccharides move through different secretory pathways journal October 2006
Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants journal March 2011
Cell Surface- and Rho GTPase-Based Auxin Signaling Controls Cellular Interdigitation in Arabidopsis journal October 2010
High-Affinity Auxin Transport by the AUX1 Influx Carrier Protein journal June 2006
ARF GEF-Dependent Transcytosis and Polar Delivery of PIN Auxin Carriers in Arabidopsis journal April 2008
Dynamic Coordination of Cytoskeletal and Cell Wall Systems during Plant Cell Morphogenesis journal September 2009
A ROP GTPase-Dependent Auxin Signaling Pathway Regulates the Subcellular Distribution of PIN2 in Arabidopsis Roots journal July 2012
ABP1 and ROP6 GTPase Signaling Regulate Clathrin-Mediated Endocytosis in Arabidopsis Roots journal July 2012
Plant Development Is Regulated by a Family of Auxin Receptor F Box Proteins journal July 2005
Cytoplasmic Streaming Velocity as a Plant Size Determinant journal November 2013
Actin dynamics in the cortical array of plant cells journal December 2013
Cell shape development in plants journal December 2004
The Arabidopsis F-box protein TIR1 is an auxin receptor journal May 2005
The F-box protein TIR1 is an auxin receptor journal May 2005
The epidermis both drives and restricts plant shoot growth journal March 2007
A novel sensor to map auxin response and distribution at high spatio-temporal resolution journal January 2012
A combinatorial TIR1/AFB–Aux/IAA co-receptor system for differential sensing of auxin journal April 2012
Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity journal May 2015
Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis journal March 2015
Embryonic lethality of Arabidopsis abp1-1 is caused by deletion of the adjacent BSM gene journal November 2015
Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method journal June 2006
Preparation of plants for developmental and cellular imaging by light-sheet microscopy journal July 2015
Growth of the plant cell wall journal November 2005
AUX1-mediated root hair auxin influx governs SCFTIR1/AFB-type Ca2+ signaling journal March 2018
Rapid and reversible root growth inhibition by TIR1 auxin signalling journal June 2018
Arabidopsis actin gene ACT7 plays an essential role in germination and root growth journal January 2003
Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes journal March 2008
Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells journal March 2010
Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism journal March 2012
Rice actin-binding protein RMD is a key link in the auxin-actin regulatory loop that controls cell growth journal June 2014
Auxin transport sites are visualized in planta using fluorescent auxin analogs journal July 2014
Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development journal February 2015
Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression journal December 2015
Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport. journal July 1996
Activation and repression of transcription by auxin-response factors journal May 1999
Histological analysis of adventitious rooting in Arabidopsis thaliana (L.) Heynh seedlings journal January 2003
Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array journal January 2009
The availability of filament ends modulates actin stochastic dynamics in live plant cells journal April 2014
The AUX1 LAX family of auxin influx carriers is required for the establishment of embryonic root cell organization in Arabidopsis thaliana journal December 2009
AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues journal April 1999
Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. journal March 1995
Keeping it all together: auxin–actin crosstalk in plant development journal June 2015
Capturing in vivo Dynamics of the Actin Cytoskeleton Stimulated by Auxin or Light journal July 2004
Quantitative analyses of the plant cytoskeleton reveal underlying organizational principles journal August 2014
Auxin Control of Root Development journal April 2010
A New Algorithm for Computational Image Analysis of Deformable Motion at High Spatial and Temporal Resolution Applied to Root Growth. Roughly Uniform Elongation in the Meristem and Also, after an Abrupt Acceleration, in the Elongation Zone journal July 2003
Transport of the Two Natural Auxins, Indole-3-Butyric Acid and Indole-3-Acetic Acid, in Arabidopsis journal October 2003
A Green Fluorescent Protein Fusion to Actin-Binding Domain 2 of Arabidopsis Fimbrin Highlights New Features of a Dynamic Actin Cytoskeleton in Live Plant Cells journal November 2004
The Binding of Auxin to the Arabidopsis Auxin Influx Transporter AUX1 journal July 2008
Auxin Stimulates Its Own Transport by Shaping Actin Filaments journal July 2009
Arabidopsis Myosin XI: A Motor Rules the Tracks journal September 2014
Rearrangement of Actin Microfilaments in Plant Root Hairs Responding to Rhizobium etli Nodulation Signals journal March 1998
Analysis of Cell Division and Elongation Underlying the Developmental Acceleration of Root Growth in Arabidopsis thaliana journal April 1998
STUNTED PLANT 1 Mediates Effects of Cytokinin, But Not of Auxin, on Cell Division and Expansion in the Root of Arabidopsis journal December 2000
Profilin-Dependent Nucleation and Assembly of Actin Filaments Controls Cell Elongation in Arabidopsis journal November 2015
Effects of Auxins on PIN-FORMED2 (PIN2) Dynamics Are Not Mediated by Inhibiting PIN2 Endocytosis journal August 2016
The Actin Cytoskeleton: Functional Arrays for Cytoplasmic Organization and Cell Shape Control journal November 2017
Myosins XI Are Involved in Exocytosis of Cellulose Synthase Complexes journal January 2019
An Auxin Transport Inhibitor Targets Villin-Mediated Actin Dynamics to Regulate Polar Auxin Transport journal July 2019
The aux1 Mutation of Arabidopsis Confers Both Auxin and Ethylene Resistance journal November 1990
Unstable F-Actin Specifies the Area and Microtubule Direction of Cell Expansion in Arabidopsis Root Hairs journal December 2002
Structure-Function Analysis of the Presumptive Arabidopsis Auxin Permease AUX1 journal October 2004
Subcellular Trafficking of the Arabidopsis Auxin Influx Carrier AUX1 Uses a Novel Pathway Distinct from PIN1 journal November 2006
A Single Vegetative Actin Isovariant Overexpressed under the Control of Multiple Regulatory Sequences Is Sufficient for Normal Arabidopsis Development journal March 2009
Myosin XI Is Essential for Tip Growth in Physcomitrella patens journal June 2010
Natural Variation of Transcriptional Auxin Response Networks in Arabidopsis thaliana journal July 2010
RICE MORPHOLOGY DETERMINANT Encodes the Type II Formin FH5 and Regulates Rice Morphogenesis journal February 2011
BENT UPPERMOST INTERNODE1 Encodes the Class II Formin FH5 Crucial for Actin Organization and Rice Development journal February 2011
AUXIN BINDING PROTEIN1: The Outsider journal June 2011
SCAR Mediates Light-Induced Root Elongation in Arabidopsis through Photoreceptors and Proteasomes journal October 2011
Arabidopsis Actin Depolymerizing Factor4 Modulates the Stochastic Dynamic Behavior of Actin Filaments in the Cortical Array of Epidermal Cells journal October 2011
Capping Protein Modulates the Dynamic Behavior of Actin Filaments in Response to Phosphatidic Acid in Arabidopsis journal September 2012
Systems Analysis of Auxin Transport in the Arabidopsis Root Apex journal March 2014
ACTIN DEPOLYMERIZING FACTOR4 Regulates Actin Dynamics during Innate Immune Signaling in Arabidopsis journal January 2014
TWISTED DWARF1 Mediates the Action of Auxin Transport Inhibitors on Actin Cytoskeleton Dynamics journal April 2016
T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum journal July 1991
Auxin, actin and growth of the Arabidopsis thaliana primary root: Auxin and actin interaction journal April 2007
Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells journal January 2010
Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis: Calcium and auxin signaling journal December 2010
Growth Inhibition and Recovery in Roots Following Temporary Treatment with Auxin journal February 1968
TRANSPORT OF INDOLEACETIC ACID IN PLANT CELLS IN RELATION TO pH AND ELECTRICAL POTENTIAL GRADIENTS, AND ITS SIGNIFICANCE FOR POLAR IAA TRANSPORT journal March 1975
My body is a cage: mechanisms and modulation of plant cell growth journal August 2013
The carrier AUXIN RESISTANT (AUX1) dominates auxin flux into Arabidopsis protoplasts journal July 2014
Cell Surface ABP1-TMK Auxin-Sensing Complex Activates ROP GTPase Signaling journal February 2014
Arabidopsis AUX1 Gene: A Permease-Like Regulator of Root Gravitropism journal August 1996
Control of the Actin Cytoskeleton in Plant cell Growth journal June 2006
Skewing in Arabidopsis roots involves disparate environmental signaling pathways journal February 2017
Brassinosteroid perception in the epidermis controls root meristem size journal January 2011
Strategies of actin reorganisation in plant cells journal August 2010
Auxin transporters and binding proteins at a glance journal January 2015
ROP GTPase-Dependent Actin Microfilaments Promote PIN1 Polarization by Localized Inhibition of Clathrin-Dependent Endocytosis journal April 2012
Regulator or Driving Force? The Role of Turgor Pressure in Oscillatory Plant Cell Growth journal April 2011
Transcription of DWARF4 Plays a Crucial Role in Auxin-Regulated Root Elongation in Addition to Brassinosteroid Homeostasis in Arabidopsis thaliana journal August 2011
Stability of IAA and IBA in Nutrient Medium to Several Tissue Culture Procedures journal July 1990
Bundling actin filaments from membranes: some novel players journal January 2012
AUX/LAX family of auxin influx carriers—an overview journal January 2012
Root Apex Transition Zone As Oscillatory Zone journal January 2013
No Stress! Relax! Mechanisms Governing Growth and Shape in Plant Cells journal March 2014
The Root Apex of Arabidopsis thaliana Consists of Four Distinct Zones of Growth Activities : Meristematic Zone, Transition Zone, Fast Elongation Zone and Growth Terminating Zone journal November 2006
Critical role of actin bundling in plant cell morphogenesis journal May 2010
Probing the actin-auxin oscillator journal February 2010
Uniform auxin triggers the Rho GTPase-dependent formation of interdigitation patterns in pavement cells journal July 2011