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Mol. Biol. Cell 17 (4): 1946-1958

Copyright © 2006 by The American Society for Cell Biology.

Heterodimeric Capping Protein from Arabidopsis Is Regulated by Phosphatidic Acid

Shanjin Huang *, Lisa Gao *, Laurent Blanchoin {dagger}, and Christopher J. Staiger *

* Department of Biological Sciences and The Bindley Bioscience Center, Purdue University, West Lafayette, IN 47907-2064
{dagger} Laboratoire de Physiologie Cellulaire Végétale, Commissariat à l'Energie Atomique/Centre National de la Recherche Scientifique/Université Joseph Fourier, F38054 Grenoble, France

Received for publication September 6, 2005. Revision received December 13, 2005. Accepted for publication January 17, 2006.

Monitoring Editor: Thomas Pollard

Abstract: The cytoskeleton is a key regulator of morphogenesis, sexual reproduction, and cellular responses to extracellular stimuli. Changes in the cellular architecture are often assumed to require actin-binding proteins as stimulus-response modulators, because many of these proteins are regulated directly by binding to intracellular second messengers or signaling phospholipids. Phosphatidic acid (PA) is gaining widespread acceptance as a major, abundant phospholipid in plants that is required for pollen tube tip growth and mediates responses to osmotic stress, wounding, and phytohormones; however, the number of identified effectors of PA is rather limited. Here we demonstrate that exogenous PA application leads to significant increases in filamentous actin levels in Arabidopsis suspension cells and poppy pollen grains. To investigate further these lipid-induced changes in polymer levels, we analyzed the properties of a key regulator of actin filament polymerization, the heterodimeric capping protein from Arabidopsis thaliana (AtCP). AtCP binds to PA with a Kd value of 17 µM and stoichiometry of ~1:2. It also binds well to PtdIns(4,5)P2, but not to several other phosphoinositide or acidic phospholipids. The interaction with PA inhibited the actin-binding activity of CP. In the presence of PA, CP is unable to block the barbed or rapidly growing and shrinking end of actin filaments. Precapped filament barbed ends can also be uncapped by addition of PA, allowing rapid filament assembly from an actin monomer pool that is buffered with profilin. The findings support a model in which the inhibition of CP activity in cells by elevated PA results in the stimulation of actin polymerization from a large pool of profilin-actin. Such regulation may be important for the response of plant cells to extracellular stimuli as well as for the normal process of pollen tube tip growth.

This article was published online ahead of print in MBC in Press (http://www.molbiolcell.org/cgi/doi/10.1091/mbc.E05-09-0840) on January 25, 2006.

Address correspondence to: Christopher J. Staiger (cstaiger{at}bilbo.bio.purdue.edu).

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