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J. Biol. Chem., Vol. 279, Issue 22, 23364-23375, May 28, 2004

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A Gelsolin-like Protein from Papaver rhoeas Pollen (PrABP80) Stimulates Calcium-regulated Severing and Depolymerization of Actin Filaments^*

Shanjin Huang, Laurent Blanchoin¶, Faisal Chaudhry, Vernonica E. Franklin-Tong||, and Christopher J. Staiger**

From the Department of Biological Sciences and The Purdue Motility Group, Purdue University, West Lafayette, Indiana 47907-2064, the Laboratoire de Physiologie Cellulaire Végétale, Commissariat à l'Energie Atomique (CEA)/CNRS/Université Joseph Fourier, CEA F38054 Grenoble, France, and the ^||School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom

The cytoskeleton is a key regulator of plant morphogenesis, sexual reproduction, and cellular responses to extracellular stimuli. During the self-incompatibility response of Papaver rhoeas L. (field poppy) pollen, the actin filament network is rapidly depolymerized by a flood of cytosolic free Ca²⁺ that results in cessation of tip growth and prevention of fertilization. Attempts to model this dramatic cytoskeletal response with known pollen actin-binding proteins (ABPs) revealed that the major G-actin-binding protein profilin can account for only a small percentage of the measured depolymerization. We have identified an 80-kDa, Ca²⁺-regulated ABP from poppy pollen (PrABP80) and characterized its biochemical properties in vitro. Sequence determination by mass spectrometry revealed that PrABP80 is related to gelsolin and villin. The molecular weight, lack of filament cross-linking activity, and a potent severing activity are all consistent with PrABP80 being a plant gelsolin. Kinetic analysis of actin assembly/disassembly reactions revealed that substoichiometric amounts of PrABP80 can nucleate actin polymerization from monomers, block the assembly of profilin-actin complex onto actin filament ends, and enhance profilin-mediated actin depolymerization. Fluorescence microscopy of individual actin filaments provided compelling, direct evidence for filament severing and confirmed the actin nucleation and barbed end capping properties. This is the first direct evidence for a plant gelsolin and the first example of efficient severing by a plant ABP. We propose that PrABP80 functions at the center of the self-incompatibility response by creating new filament pointed ends for disassembly and by blocking barbed ends from profilin-actin assembly.

Received for publication, November 30, 2003 , and in revised form, March 12, 2004.

^* This work was supported by grants from the Department of Energy, Energy Biosciences Division (DE-FG02-99ER20337A01) (to C. J. S.) and from the Biotechnology and Biological Sciences Research Council, UK (to V. E. F. T.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains four supplementary time-lapse movies of actin filament severing.

^¶ Supported by an Actions Thématiques et Incitives sur Programmes et Equipes from the CNRS.

^** To whom correspondence should be addressed: Dept. of Biological Sciences, Purdue University, 333 Hansen Life Sciences Bldg., 201 S. University St., West Lafayette, IN 47907-2064. Tel.: 765-496-1769; Fax: 765-496-1496; E-mail: cstaiger{at}bilbo.bio.purdue.edu.

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