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Title: The availability of filament ends modulates actin stochastic dynamics in live plant cells

Abstract

A network of individual filaments that undergoes incessant remodeling through a process known as stochastic dynamics comprises the cortical actin cytoskeleton in plant epidermal cells. From images at high spatial and temporal resolution, it has been inferred that the regulation of filament barbed ends plays a central role in choreographing actin organization and turnover. How this occurs at a molecular level, whether different populations of ends exist in the array, and how individual filament behavior correlates with the overall architecture of the array are unknown. Here we develop an experimental system to modulate the levels of heterodimeric capping protein (CP) and examine the consequences for actin dynamics, architecture, and cell expansion. Significantly, we find that all phenotypes are the opposite for CP-overexpression (OX) cells compared with a previously characterized cp-knockdown line. Specifically, CP OX lines have fewer filament–filament annealing events, as well as reduced filament lengths and lifetimes. Further, cp-knockdown and OX lines demonstrate the existence of a subpopulation of filament ends sensitive to CP concentration. Finally, CP levels correlate with the biological process of axial cell expansion; for example, epidermal cells from hypocotyls with reduced CP are longer than wild-type cells, whereas CP OX lines have shorter cells. Onmore » the basis of these and other genetic studies in this model system, we hypothesize that filament length and lifetime positively correlate with the extent of axial cell expansion in dark-grown hypocotyls.« less

Authors:
 [1];  [1];  [1];  [2];  [2];  [3];  [4]
+ Show Author Affiliations
  1. Purdue Univ., West Lafayette, IN (United States). Dept. of Biological Sciences
  2. Volcani Center (Israel). Inst. of Plant Sciences
  3. Univ. Joseph Fourier, Grenoble (France). Comissariat a l'Energie Atomique/Centre National de la Recherche Scientifique/Institute de la Recherche Agronomique. Institut de Recherches en Technologie et Sciences pour le Vivant. Laboratoire de Physiologie Cellulaire et Végétale
  4. Purdue Univ., West Lafayette, IN (United States). Dept. of Biological Sciences; Purdue Univ., West Lafayette, IN (United States). Bindley Bioscience Center
Publication Date:
Research Org.:
Purdue Univ., West Lafayette, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division
OSTI Identifier:
1625231
Grant/Contract Number:  
FG02-04ER15526
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Biology of the Cell
Additional Journal Information:
Journal Volume: 25; Journal Issue: 8; Journal ID: ISSN 1059-1524
Publisher:
American Society for Cell Biology
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Cell Biology

Citation Formats

Li, Jiejie, Staiger, Benjamin H., Henty-Ridilla, Jessica L., Abu-Abied, Mohamad, Sadot, Einat, Blanchoin, Laurent, and Staiger, Christopher J. The availability of filament ends modulates actin stochastic dynamics in live plant cells. United States: N. p., 2014. Web. doi:10.1091/mbc.e13-07-0378.
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Li, Jiejie, Staiger, Benjamin H., Henty-Ridilla, Jessica L., Abu-Abied, Mohamad, Sadot, Einat, Blanchoin, Laurent, & Staiger, Christopher J. The availability of filament ends modulates actin stochastic dynamics in live plant cells. United States. https://doi.org/10.1091/mbc.e13-07-0378
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Li, Jiejie, Staiger, Benjamin H., Henty-Ridilla, Jessica L., Abu-Abied, Mohamad, Sadot, Einat, Blanchoin, Laurent, and Staiger, Christopher J. Tue . "The availability of filament ends modulates actin stochastic dynamics in live plant cells". United States. https://doi.org/10.1091/mbc.e13-07-0378. https://www.osti.gov/servlets/purl/1625231.
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@article{osti_1625231,
title = {The availability of filament ends modulates actin stochastic dynamics in live plant cells},
author = {Li, Jiejie and Staiger, Benjamin H. and Henty-Ridilla, Jessica L. and Abu-Abied, Mohamad and Sadot, Einat and Blanchoin, Laurent and Staiger, Christopher J.},
abstractNote = {A network of individual filaments that undergoes incessant remodeling through a process known as stochastic dynamics comprises the cortical actin cytoskeleton in plant epidermal cells. From images at high spatial and temporal resolution, it has been inferred that the regulation of filament barbed ends plays a central role in choreographing actin organization and turnover. How this occurs at a molecular level, whether different populations of ends exist in the array, and how individual filament behavior correlates with the overall architecture of the array are unknown. Here we develop an experimental system to modulate the levels of heterodimeric capping protein (CP) and examine the consequences for actin dynamics, architecture, and cell expansion. Significantly, we find that all phenotypes are the opposite for CP-overexpression (OX) cells compared with a previously characterized cp-knockdown line. Specifically, CP OX lines have fewer filament–filament annealing events, as well as reduced filament lengths and lifetimes. Further, cp-knockdown and OX lines demonstrate the existence of a subpopulation of filament ends sensitive to CP concentration. Finally, CP levels correlate with the biological process of axial cell expansion; for example, epidermal cells from hypocotyls with reduced CP are longer than wild-type cells, whereas CP OX lines have shorter cells. On the basis of these and other genetic studies in this model system, we hypothesize that filament length and lifetime positively correlate with the extent of axial cell expansion in dark-grown hypocotyls.},
doi = {10.1091/mbc.e13-07-0378},
journal = {Molecular Biology of the Cell},
number = 8,
volume = 25,
place = {United States},
year = {Tue Apr 15 00:00:00 EDT 2014},
month = {Tue Apr 15 00:00:00 EDT 2014}
}
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Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway.
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Cellular Motility Driven by Assembly and Disassembly of Actin Filaments
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Signal-Mediated Depolymerization of Actin in Pollen during the Self-Incompatibility Response
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Strategies of actin reorganisation in plant cells
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Mechanism and Function of Formins in the Control of Actin Assembly
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Latrunculin B-Induced Plant Dwarfism: Plant Cell Elongation Is F-Actin-Dependent
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Actin organization, bristle morphology, and viability are affected by actin capping protein mutations in Drosophila.
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Cellular Basis of Hypocotyl Growth in Arabidopsis thaliana
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Latrunculin B-Induced Plant Dwarfism: Plant Cell Elongation Is F-Actin-Dependent
journal, March 2001

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Capping protein levels influence actin assembly and cell motility in dictyostelium
journal, May 1995

Dynamic Coordination of Cytoskeletal and Cell Wall Systems during Plant Cell Morphogenesis
journal, September 2009

The Myosin Passenger Protein Smy1 Controls Actin Cable Structure and Dynamics by Acting as a Formin Damper
journal, August 2011

Cytoplasmic Streaming Velocity as a Plant Size Determinant
journal, November 2013

Actin dynamics in plant cells: a team effort from multiple proteins orchestrates this very fast-paced game
journal, December 2010

  • Blanchoin, Laurent; Boujemaa-Paterski, Rajaa; Henty, Jessica L.
  • Current Opinion in Plant Biology, Vol. 13, Issue 6
  • DOI: 10.1016/j.pbi.2010.09.013

Actin dynamics in the cortical array of plant cells
journal, December 2013

  • Henty-Ridilla, Jessica L.; Li, Jiejie; Blanchoin, Laurent
  • Current Opinion in Plant Biology, Vol. 16, Issue 6
  • DOI: 10.1016/j.pbi.2013.10.012

Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid
journal, September 2013

Control of actin assembly and disassembly at filament ends
journal, February 2000

Disruption of the actin cytoskeleton in yeast capping protein mutants
journal, March 1990

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Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments
journal, June 2009

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Self-organization of actin filament orientation in the dendritic-nucleation/array-treadmilling model
journal, April 2007

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  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 17
  • DOI: 10.1073/pnas.0701943104

Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth
journal, July 2009

  • Vidali, L.; van Gisbergen, P. A. C.; Guerin, C.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 32
  • DOI: 10.1073/pnas.0901170106

Arabidopsis Capping Protein (AtCP) Is a Heterodimer That Regulates Assembly at the Barbed Ends of Actin Filaments
journal, November 2003

  • Huang, Shanjin; Blanchoin, Laurent; Kovar, David R.
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Actin filaments in yeast are unstable in the absence of capping protein or fimbrin.
journal, December 1995

  • Karpova, T. S.; Tatchell, K.; Cooper, J. A.
  • Journal of Cell Biology, Vol. 131, Issue 6
  • DOI: 10.1083/jcb.131.6.1483

Actin organization, bristle morphology, and viability are affected by actin capping protein mutations in Drosophila.
journal, June 1996

  • Hopmann, R.; Cooper, J. A.; Miller, K. G.
  • Journal of Cell Biology, Vol. 133, Issue 6
  • DOI: 10.1083/jcb.133.6.1293

Molecular requirements for actin-based lamella formation in Drosophila S2 cells
journal, September 2003

  • Rogers, Stephen L.; Wiedemann, Ursula; Stuurman, Nico
  • Journal of Cell Biology, Vol. 162, Issue 6
  • DOI: 10.1083/jcb.200303023

Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array
journal, January 2009

  • Staiger, Christopher J.; Sheahan, Michael B.; Khurana, Parul
  • The Journal of Cell Biology, Vol. 184, Issue 2
  • DOI: 10.1083/jcb.200806185

Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway
journal, March 2010

  • Okreglak, Voytek; Drubin, David G.
  • Journal of Cell Biology, Vol. 188, Issue 6
  • DOI: 10.1083/jcb.200909176

Class II formin targeting to the cell cortex by binding PI(3,5)P 2 is essential for polarized growth
journal, July 2012

  • van Gisbergen, Peter A. C.; Li, Ming; Wu, Shu-Zon
  • The Journal of Cell Biology, Vol. 198, Issue 2
  • DOI: 10.1083/jcb.201112085

Profilin-mediated Competition between Capping Protein and Formin Cdc12p during Cytokinesis in Fission Yeast
journal, May 2005

  • Kovar, David R.; Wu, Jian-Qiu; Pollard, Thomas D.
  • Molecular Biology of the Cell, Vol. 16, Issue 5
  • DOI: 10.1091/mbc.e04-09-0781

Heterodimeric Capping Protein from Arabidopsis Is Regulated by Phosphatidic Acid
journal, April 2006

  • Huang, Shanjin; Gao, Lisa; Blanchoin, Laurent
  • Molecular Biology of the Cell, Vol. 17, Issue 4
  • DOI: 10.1091/mbc.e05-09-0840

AtFH1 formin mutation affects actin filament and microtubule dynamics in Arabidopsis thaliana
journal, December 2012

  • Rosero, Amparo; Žárský, Viktor; Cvrčková, Fatima
  • Journal of Experimental Botany, Vol. 64, Issue 2
  • DOI: 10.1093/jxb/ers351

Plasma Membrane-Associated SCAR Complex Subunits Promote Cortical F-Actin Accumulation and Normal Growth Characteristics in Arabidopsis Roots
journal, November 2008

  • Dyachok, Julia; Shao, Mon-Ray; Vaughn, Kevin
  • Molecular Plant, Vol. 1, Issue 6
  • DOI: 10.1093/mp/ssn059

Golgi Body Motility in the Plant Cell Cortex Correlates with Actin Cytoskeleton Organization
journal, September 2011

  • Akkerman, Miriam; Overdijk, Elysa J. R.; Schel, Jan H. N.
  • Plant and Cell Physiology, Vol. 52, Issue 10
  • DOI: 10.1093/pcp/pcr122

Patterning and Lifetime of Plasma Membrane-Localized Cellulose Synthase Is Dependent on Actin Organization in Arabidopsis Interphase Cells
journal, April 2013

  • Sampathkumar, Arun; Gutierrez, Ryan; McFarlane, Heather E.
  • Plant Physiology, Vol. 162, Issue 2
  • DOI: 10.1104/pp.113.215277

Cellular Basis of Hypocotyl Growth in Arabidopsis thaliana
journal, May 1997

Signal-Mediated Depolymerization of Actin in Pollen during the Self-Incompatibility Response
journal, September 2002

  • Snowman, Benjamin N.; Kovar, David R.; Shevchenko, Galina
  • The Plant Cell, Vol. 14, Issue 10
  • DOI: 10.1105/tpc.002998

A Single Vegetative Actin Isovariant Overexpressed under the Control of Multiple Regulatory Sequences Is Sufficient for Normal Arabidopsis Development
journal, March 2009

  • Kandasamy, Muthugapatti K.; McKinney, Elizabeth C.; Meagher, Richard B.
  • The Plant Cell, Vol. 21, Issue 3
  • DOI: 10.1105/tpc.108.061960

Myosin XI Is Essential for Tip Growth in Physcomitrella patens
journal, June 2010

  • Vidali, Luis; Burkart, Graham M.; Augustine, Robert C.
  • The Plant Cell, Vol. 22, Issue 6
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    Works referencing / citing this record:

    Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity
    journal, May 2015

    • Li, Jiejie; Henty-Ridilla, Jessica L.; Staiger, Benjamin H.
    • Nature Communications, Vol. 6, Issue 1
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    Auxin‐induced actin cytoskeleton rearrangements require AUX1
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    • Arieti, Ruthie S.; Staiger, Christopher J.
    • New Phytologist, Vol. 226, Issue 2
    • DOI: 10.1111/nph.16382

    Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity
    journal, May 2015

    • Li, Jiejie; Henty-Ridilla, Jessica L.; Staiger, Benjamin H.
    • Nature Communications, Vol. 6, Issue 1
    • DOI: 10.1038/ncomms8206
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