DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array

Journal Article · · Journal of Cell Biology
 [1];  [2];  [3];  [4];  [5];  [6]
  1. Purdue Univ., West Lafayette, IN (United States). Dept. of Biological Sciences. The Bindley Bioscience Center; DOE/OSTI
  2. Univ. of Newcastle, NSW (Australia). School of Environmental and Life Sciences. Plant Science Group; Univ. of Newcastle, NSW (Australia). ARC Centre of Excellence for Integrative Legume Research
  3. Purdue Univ., West Lafayette, IN (United States). Dept. of Biological Sciences. The Bindley Bioscience Center
  4. Purdue Univ., West Lafayette, IN (United States). Dept. of Biological Sciences.
  5. Univ. of Newcastle, NSW (Australia). School of Environmental and Life Sciences. Plant Science Group
  6. Univ. Joseph Fourier, Grenoble (France). Institut National de la Recherche Agronomique. Centre National de la Recherche Scientifique. Commissariat à l'Energie Atomique. Laboratoire de Physiologie Cellulaire Végétale. Institut de Recherches en Technologie et Sciences pour le Vivant – iRTSV

Metazoan cells harness the power of actin dynamics to create cytoskeletal arrays that stimulate protrusions and drive intracellular organelle movements. In plant cells, the actin cytoskeleton is understood to participate in cell elongation; however, a detailed description and molecular mechanism(s) underpinning filament nucleation, growth, and turnover are lacking. Here, we use variable-angle epifluorescence microscopy (VAEM) to examine the organization and dynamics of the cortical cytoskeleton in growing and nongrowing epidermal cells. One population of filaments in the cortical array, which most likely represent single actin filaments, is randomly oriented and highly dynamic. These filaments grow at rates of 1.7 µm/s, but are generally short-lived. Instead of depolymerization at their ends, actin filaments are disassembled by severing activity. Remodeling of the cortical actin array also features filament buckling and straightening events. These observations indicate a mechanism inconsistent with treadmilling. Instead, cortical actin filament dynamics resemble the stochastic dynamics of an in vitro biomimetic system for actin assembly.

Research Organization:
Purdue Univ., West Lafayette, IN (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
FG02-04ER15526
OSTI ID:
1625151
Journal Information:
Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 2 Vol. 184; ISSN 0021-9525
Publisher:
Rockefeller University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (101)

Living markers for actin block myosin-dependent motility of plant organelles and auxin journal January 2007
Is 2,3-butanedione monoxime an effective inhibitor of myosin-based activities in plant cells? journal March 1999
Actin-filament-dependent remodeling of the vacuole in cultured mesophyll protoplasts journal April 2007
A Novel Localization Pattern for an EB1-like Protein Links Microtubule Dynamics to Endomembrane Organization journal November 2003
The Actin-Interacting Protein AIP1 Is Essential for Actin Organization and Plant Development journal February 2004
Actin-Filament Stochastic Dynamics Mediated by ADF/Cofilin journal May 2007
Plant organelle positioning journal December 2004
Transport and secretion in plant–microbe interactions journal December 2007
Actin microfilament dynamics and actin side-binding proteins in plants journal December 2007
Cortical microtubule arrays in the Arabidopsis seedling journal February 2008
New Directions for Fluorescent Speckle Microscopy journal September 2002
Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells journal January 2007
Xenopus Actin-interacting Protein 1 (XAip1) Enhances Cofilin Fragmentation of Filaments by Capping Filament Ends journal November 2002
Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. journal December 1986
Arp2/3 Complex and Actin Depolymerizing Factor/Cofilin in Dendritic Organization and Treadmilling of Actin Filament Array in Lamellipodia journal May 1999
The Motility of Chara corallina Myosin was Inhibited Reversibly by 2,3-Butanedione Monoxime (BDM) journal September 2004
Actin Microfilaments Regulate Vacuolar Structures and Dynamics: Dual Observation of Actin Microfilaments and Vacuolar Membrane in Living Tobacco BY-2 Cells journal July 2006
Green Fluorescent Protein-mTalin Causes Defects in Actin Organization and Cell Expansion in Arabidopsis and Inhibits Actin Depolymerizing Factor's Actin Depolymerizing Activity in Vitro journal November 2004
Comparison of the Dynamics and Functional Redundancy of the Arabidopsis Dynamin-Related Isoforms DRP1A and DRP1C during Plant Development journal March 2008
Cellular Basis of Hypocotyl Growth in Arabidopsis thaliana journal May 1997
Stop-and-Go Movements of Plant Golgi Stacks Are Mediated by the Acto-Myosin System journal December 1999
Villin-Like Actin-Binding Proteins Are Expressed Ubiquitously in Arabidopsis journal January 2000
Regulation of the Pollen-Specific Actin-Depolymerizing Factor LlADF1 journal October 2002
Encounters between Dynamic Cortical Microtubules Promote Ordering of the Cortical Array through Angle-Dependent Modifications of Microtubule Behavior journal November 2004
Arabidopsis VILLIN1 Generates Actin Filament Cables That Are Resistant to Depolymerization journal January 2005
The Formin Homology 1 Domain Modulates the Actin Nucleation and Bundling Activity of Arabidopsis FORMIN1 journal July 2005
ACTIN BINDING PROTEIN29 from Lilium Pollen Plays an Important Role in Dynamic Actin Remodeling journal June 2007
Dynamics of Arabidopsis Dynamin-Related Protein 1C and a Clathrin Light Chain at the Plasma Membrane journal May 2008
Latrunculin B Has Different Effects on Pollen Germination and Tube Growth journal December 1999
ADF Proteins Are Involved in the Control of Flowering and Regulate F-Actin Organization, Cell Expansion, and Organ Growth in Arabidopsis journal June 2001
Variable-angle epifluorescence microscopy: a new way to look at protein dynamics in the plant cell cortex journal January 2008
Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C‐ and N‐termini of the fimbrin actin‐binding domain 2 journal November 2007
Two Distinct Actin Networks Drive the Protrusion of Migrating Cells journal September 2004
Assembly Mechanism of the Contractile Ring for Cytokinesis by Fission Yeast journal December 2007
Control of the Actin Cytoskeleton in Plant cell Growth journal June 2006
Molecular Mechanisms Controlling Actin Filament Dynamics in Nonmuscle Cells journal June 2000
Spatial Control of cell Expansion by the Plant Cytoskeleton journal November 2005
A myosin inhibitor impairs auxin-induced cell division text January 2003
Living markers for actin block myosin-dependent motility of plant organelles and auxin journal January 2007
Mechanism of inhibition of cytoplasmic streaming by a myosin inhibitor, 2,3-butanedione monoxime journal March 2000
Is 2,3-butanedione monoxime an effective inhibitor of myosin-based activities in plant cells? journal March 1999
A myosin inhibitor impairs auxin-induced cell division journal December 2003
Actin-filament-dependent remodeling of the vacuole in cultured mesophyll protoplasts journal April 2007
Recent progress in living cell imaging of plant cytoskeleton and vacuole using fluorescent-protein transgenic lines and three-dimensional imaging journal April 2007
New Directions for Fluorescent Speckle Microscopy journal September 2002
Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells journal November 1998
Plant formins: Diverse isoforms and unique molecular mechanism journal February 2010
A Novel Localization Pattern for an EB1-like Protein Links Microtubule Dynamics to Endomembrane Organization journal November 2003
The Actin-Interacting Protein AIP1 Is Essential for Actin Organization and Plant Development journal January 2004
The Actin-Interacting Protein AIP1 Is Essential for Actin Organization and Plant Development journal February 2004
Spatial and Temporal Relationships between Actin-Filament Nucleation, Capping, and Disassembly journal March 2007
Actin-Filament Stochastic Dynamics Mediated by ADF/Cofilin journal May 2007
GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings journal July 2005
Plant organelle positioning journal December 2004
Actin dynamics: old friends with new stories journal December 2006
Cytoskeleton and cell wall function in penetration resistance journal August 2007
Transport and secretion in plant–microbe interactions journal December 2007
Actin microfilament dynamics and actin side-binding proteins in plants journal December 2007
Cortical microtubule arrays in the Arabidopsis seedling journal February 2008
2,3-Butanedione monoxime (BDM) as a myosin inhibitor journal August 2002
Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells journal January 2007
Xenopus Actin-interacting Protein 1 (XAip1) Enhances Cofilin Fragmentation of Filaments by Capping Filament Ends journal November 2002
Arabidopsis Capping Protein (AtCP) Is a Heterodimer That Regulates Assembly at the Barbed Ends of Actin Filaments journal November 2003
Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. journal December 1986
Arp2/3 Complex and Actin Depolymerizing Factor/Cofilin in Dendritic Organization and Treadmilling of Actin Filament Array in Lamellipodia journal May 1999
Heterodimeric Capping Protein from Arabidopsis Is Regulated by Phosphatidic Acid journal April 2006
Establishment of Polarity during Organization of the Acentrosomal Plant Cortical Microtubule Array journal March 2006
Identification of Arabidopsis Cyclase-associated Protein 1 as the First Nucleotide Exchange Factor for Plant Actin journal August 2007
The Motility of Chara corallina Myosin was Inhibited Reversibly by 2,3-Butanedione Monoxime (BDM) journal September 2004
Actin Microfilaments Regulate Vacuolar Structures and Dynamics: Dual Observation of Actin Microfilaments and Vacuolar Membrane in Living Tobacco BY-2 Cells journal July 2006
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
Green Fluorescent Protein-mTalin Causes Defects in Actin Organization and Cell Expansion in Arabidopsis and Inhibits Actin Depolymerizing Factor's Actin Depolymerizing Activity in Vitro journal November 2004
Comparison of the Dynamics and Functional Redundancy of the Arabidopsis Dynamin-Related Isoforms DRP1A and DRP1C during Plant Development journal March 2008
Cellular Basis of Hypocotyl Growth in Arabidopsis thaliana journal May 1997
Stop-and-Go Movements of Plant Golgi Stacks Are Mediated by the Acto-Myosin System journal December 1999
Villin-Like Actin-Binding Proteins Are Expressed Ubiquitously in Arabidopsis journal January 2000
ADF Proteins Are Involved in the Control of Flowering and Regulate F-Actin Organization, Cell Expansion, and Organ Growth in Arabidopsis journal June 2001
Regulation of the Pollen-Specific Actin-Depolymerizing Factor LlADF1 journal October 2002
Encounters between Dynamic Cortical Microtubules Promote Ordering of the Cortical Array through Angle-Dependent Modifications of Microtubule Behavior journal November 2004
Arabidopsis VILLIN1 Generates Actin Filament Cables That Are Resistant to Depolymerization journal January 2005
The Formin Homology 1 Domain Modulates the Actin Nucleation and Bundling Activity of Arabidopsis FORMIN1 journal July 2005
ACTIN BINDING PROTEIN29 from Lilium Pollen Plays an Important Role in Dynamic Actin Remodeling journal June 2007
Dynamics of Arabidopsis Dynamin-Related Protein 1C and a Clathrin Light Chain at the Plasma Membrane journal May 2008
Latrunculin B Has Different Effects on Pollen Germination and Tube Growth journal December 1999
ADF Proteins Are Involved in the Control of Flowering and Regulate F-Actin Organization, Cell Expansion, and Organ Growth in Arabidopsis journal June 2001
Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays: Microtubule dynamics journal September 2007
Variable-angle epifluorescence microscopy: a new way to look at protein dynamics in the plant cell cortex journal January 2008
Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C‐ and N‐termini of the fimbrin actin‐binding domain 2 journal November 2007
Sustained Microtubule Treadmilling in Arabidopsis Cortical Arrays journal June 2003
Two Distinct Actin Networks Drive the Protrusion of Migrating Cells journal September 2004
Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules journal June 2006
Assembly Mechanism of the Contractile Ring for Cytokinesis by Fission Yeast journal December 2007
Control of the Actin Cytoskeleton in Plant cell Growth journal June 2006
Microtubule Dynamics and Organization in the Plant Cortical Array journal June 2006
Molecular Mechanisms Controlling Actin Filament Dynamics in Nonmuscle Cells journal June 2000
Spatial Control of cell Expansion by the Plant Cytoskeleton journal November 2005
In vivoanalysis of interactions between GFP-labeled microfilaments and plastid stromules journal January 2004
Latrunculin B Has Different Effects on Pollen Germination and Tube Growth journal December 1999
ADF Proteins Are Involved in the Control of Flowering and Regulate F-Actin Organization, Cell Expansion, and Organ Growth in Arabidopsis journal June 2001
A myosin inhibitor impairs auxin-induced cell division text January 2003
Imaging of plant dynamin-related proteins and clathrin around the plasma membrane by variable incidence angle fluorescence microscopy journal January 2007

Cited By (67)

Differential sublocalization of actin variants within the nucleus journal October 2010
Recent advances in understanding the molecular mechanism of chloroplast photorelocation movement journal April 2014
Quantitative Analysis of Actin Turnover in Listeria Comet Tails: Evidence for Catastrophic Filament Turnover journal October 2010
Dynamic Coordination of Cytoskeletal and Cell Wall Systems during Plant Cell Morphogenesis journal September 2009
Actin dynamics in the cortical array of plant cells journal December 2013
DeFiNe: an optimisation-based method for robust disentangling of filamentous networks journal December 2015
Correction for Breuer et al., System-wide organization of actin cytoskeleton determines organelle transport in hypocotyl plant cells journal July 2017
Turnover of branched actin filament networks by stochastic fragmentation with ADF/cofilin journal July 2011
The availability of filament ends modulates actin stochastic dynamics in live plant cells journal April 2014
2,4-Dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal dynamics journal June 2014
Arabidopsis FIM5 decorates apical actin filaments and regulates their organization in the pollen tube journal April 2016
Application of Lifeact Reveals F-Actin Dynamics in Arabidopsis thaliana and the Liverwort, Marchantia polymorpha journal April 2009
Auxin-Induced Actin Cytoskeleton Rearrangements Require AUX1 posted_content May 2019
Establishing the role of SINE proteins in regulating stomatal dynamics in Arabidopsis thaliana posted_content January 2019
Actin kinetics shapes cortical network structure and mechanics journal April 2016
Quantitative imaging strategies pave the way for testable biological concepts journal February 2011
Fluorescent labelling of the actin cytoskeleton in plants using a cameloid antibody journal January 2014
SCARN a Novel Class of SCAR Protein That Is Required for Root-Hair Infection during Legume Nodulation journal October 2015
Lifeact-mEGFP Reveals a Dynamic Apical F-Actin Network in Tip Growing Plant Cells journal May 2009
Actin Turnover Is Required for Myosin-Dependent Mitochondrial Movements in Arabidopsis Root Hairs journal June 2009
Myosin XIK of Arabidopsis thaliana Accumulates at the Root Hair Tip and Is Required for Fast Root Hair Growth journal October 2013
Quantitative Evaluation of Stomatal Cytoskeletal Patterns during the Activation of Immune Signaling in Arabidopsis thaliana journal July 2016
The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns journal April 2013
Structural and biomechanical basis of mitochondrial movement in eukaryotic cells journal October 2013
Fluorescent tags to explore cell wall structure and dynamics journal January 2012
Bundling actin filaments from membranes: some novel players journal January 2012
ARP2/3-dependent growth in the plant kingdom: SCARs for life journal January 2013
ARP2/3 localization in Arabidopsis leaf pavement cells: a diversity of intracellular pools and cytoskeletal interactions journal January 2013
Brassinosteroids Inhibit Autotropic Root Straightening by Modifying Filamentous-Actin Organization and Dynamics journal February 2020
Guard Cell Microfilament Analyzer Facilitates the Analysis of the Organization and Dynamics of Actin Filaments in Arabidopsis Guard Cells journal June 2019
Effects of Endogenous Signals and Fusarium oxysporum on the Mechanism Regulating Genistein Synthesis and Accumulation in Yellow Lupine and Their Impact on Plant Cell Cytoskeleton journal August 2014
Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants journal January 2020
Fluorescent protein-based reporters of the actin cytoskeleton in living plant cells: Fluorophore variant, actin binding domain, and promoter considerations: Imaging Actin in Living Plants journal April 2014
Visualizing and Quantifying In Vivo Cortical Cytoskeleton Structure and Dynamics book January 2019
PCaP2 regulates nuclear positioning in growing Arabidopsis thaliana root hairs by modulating filamentous actin organization journal May 2015
Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity journal May 2015
Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells journal March 2010
AP3M harbors actin filament binding activity that is crucial for vacuole morphology and stomatal closure in Arabidopsis journal August 2019
Cytoskeletal Components Define Protein Location to Membrane Microdomains* journal September 2015
Class II formin targeting to the cell cortex by binding PI(3,5)P 2 is essential for polarized growth journal July 2012
The availability of filament ends modulates actin stochastic dynamics in live plant cells journal April 2014
AtFH1 formin mutation affects actin filament and microtubule dynamics in Arabidopsis thaliana journal December 2012
Arabidopsis FIM5 decorates apical actin filaments and regulates their organization in the pollen tube journal April 2016
Application of Lifeact Reveals F-Actin Dynamics in Arabidopsis thaliana and the Liverwort, Marchantia polymorpha journal April 2009
Spatial and Temporal Expression of Actin Depolymerizing Factors ADF7 and ADF10 during Male Gametophyte Development in Arabidopsis thaliana journal June 2011
Golgi Body Motility in the Plant Cell Cortex Correlates with Actin Cytoskeleton Organization journal September 2011
Balance of Mechanical Forces Drives Endothelial Gap Formation and May Facilitate Cancer and Immune-Cell Extravasation posted_content January 2018
Auxin-Induced Actin Cytoskeleton Rearrangements Require AUX1 posted_content May 2019
Establishing the role of SINE proteins in regulating stomatal dynamics in Arabidopsis thaliana posted_content January 2019
The reorganization of actin filaments is required for vacuolar fusion of guard cells during stomatal opening in Arabidopsis: Actin filament dynamics involved in vacuolar fusion journal September 2012
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
Building bridges: formin1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton: AtFH1 links the cell wall and actin cytoskeleton journal March 2011
Arabidopsis VILLIN2 and VILLIN3 act redundantly in sclerenchyma development via bundling of actin filaments: Villins and sclerenchyma development journal June 2012
Evolutionary Cell Biology of Proteins from Protists to Humans and Plants journal August 2017
From filaments to function: The role of the plant actin cytoskeleton in pathogen perception, signaling and immunity: Actin-based immune signaling in plants journal December 2015
Expression polymorphism at the ARPC 4 locus links the actin cytoskeleton with quantitative disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana journal December 2018
Auxin‐induced actin cytoskeleton rearrangements require AUX1 journal February 2020
An actin-depolymerizing factor from the halophyte smooth cordgrass, Spartina alterniflora ( SaADF2 ), is superior to its rice homolog ( OsADF2 ) in conferring drought and salt tolerance when constitutively overexpressed in rice journal June 2018
Actin kinetics shapes cortical network structure and mechanics journal April 2016
Actin Dynamics, Architecture, and Mechanics in Cell Motility journal January 2014
Variable-angle epifluorescence microscopy characterizes protein dynamics in the vicinity of plasma membrane in plant cells journal March 2018
Balance of mechanical forces drives endothelial gap formation and may facilitate cancer and immune-cell extravasation journal May 2019
SCARN a Novel Class of SCAR Protein That Is Required for Root-Hair Infection during Legume Nodulation journal October 2015
The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns journal April 2013
Guard Cell Microfilament Analyzer Facilitates the Analysis of the Organization and Dynamics of Actin Filaments in Arabidopsis Guard Cells journal June 2019
Effects of Endogenous Signals and Fusarium oxysporum on the Mechanism Regulating Genistein Synthesis and Accumulation in Yellow Lupine and Their Impact on Plant Cell Cytoskeleton journal August 2014
Balance of Mechanical Forces Drives Endothelial Gap Formation and May Facilitate Cancer and Immune-Cell Extravasation text January 2018