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Signal-Mediated Depolymerization Of Actin In Pollen During The Self-Incompatibility Response Article, Publication Date, And Citation Information Can Be Found At Www.plantcell.org/cgi/doi/10.1105/tpc.002998.

B. N. Snowman, D. Kovar, G. Shevchenko, V. Franklin-Tong, C. Staiger
Published 2002 · Biology, Medicine

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Signal perception and the integration of signals into networks that effect cellular changes is essential for all cells. The self-incompatibility (SI) response in field poppy pollen triggers a Ca2+-dependent signaling cascade that results in the inhibition of incompatible pollen. SI also stimulates dramatic alterations in the actin cytoskeleton. By measuring the amount of filamentous (F-) actin in pollen before and during the SI response, we demonstrate that SI stimulates a rapid and large reduction in F-actin level that is sustained for at least 1 h. This represents quantitative evidence for stimulus-mediated depolymerization of F-actin in plant cells by a defined biological stimulus. Surprisingly, there are remarkably few examples of sustained reductions in F-actin levels stimulated by a biologically relevant ligand. Actin depolymerization also was achieved in pollen by treatments that increase cytosolic free Ca2+ artificially, providing evidence that actin is a target for the Ca2+ signals triggered by the SI response. By determining the cellular concentrations and binding constants for native profilin from poppy pollen, we show that profilin has Ca2+-dependent monomeric actin-sequestering activity. Although profilin is likely to contribute to stimulus-mediated actin depolymerization, our data suggest a role for additional actin binding proteins. We propose that Ca2+-mediated depolymerization of F-actin may be a mechanism whereby SI-induced tip growth inhibition is achieved.
This paper references
Franklin-Tong and Signal-Mediated Depolymerization of Actin in Pollen during the Self-Incompatibility Response
N Benjamin
10.1105/tpc.11.12.2349
Latrunculin B Has Different Effects on Pollen Germination and Tube Growth
B. C. Gibbon (1999)
10.1105/tpc.8.8.1305
Growth of Pollen Tubes of Papaver rhoeas Is Regulated by a Slow-Moving Calcium Wave Propagated by Inositol 1,4,5-Trisphosphate.
V. E. Franklin-Tong (1996)
Free Ca2+ Gradient in Growing Pollen Tubes of Lillium
D. Miller (1992)
10.1006/DBIO.1996.0060
Tip-localized calcium entry fluctuates during pollen tube growth.
E. S. Pierson (1996)
10.1105/tpc.12.7.1239
Alterations in the Actin Cytoskeleton of Pollen Tubes Are Induced by the Self-Incompatibility Reaction in Papaver rhoeas
A. Geitmann (2000)
10.1016/0020-711x(94)90115-5
Guidebook to cytoskeletal and motor proteins
T. Kreis (1999)
Ser6 in the maize actindepolymerizing factor, ZmADF3, is phosphorylated by a calcium
A. P. Smertenko (1998)
Profilin
B. C. Gibbon (2000)
10.1016/0012-1606(91)90278-B
A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes.
K. Rathore (1991)
10.1002/(SICI)1097-4644(19991215)75:4<686::AID-JCB14>3.0.CO;2-F
Alterations of the actin polymerization status as an apoptotic morphological effector in HL‐60 cells
J. Rao (1999)
10.1016/S0014-5793(01)02528-5
Phosphorylation of plant actin‐depolymerising factor by calmodulin‐like domain protein kinase
E. Allwood (2001)
10.1146/ANNUREV.CELLBIO.17.1.159
Polarized cell growth in higher plants.
P. Hepler (2001)
Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum.
M. Messerli (1997)
10.1046/J.1365-313X.2000.00907.X
AtFim1 is an actin filament crosslinking protein from Arabidopsis thaliana.
D. Kovar (2000)
10.1007/s004970050141
Identification and cloning of related self-incompatibility S-genes in Papaver rhoeas and Papaver nudicaule
S. Kurup (1998)
10.1006/EXCR.1998.4256
Activation of cysteine proteases in cowpea plants during the hypersensitive response--a form of programmed cell death.
I. D'Silva (1998)
10.1152/AJPCELL.1991.260.1.C9
Vasopressin depolymerizes F-actin in toad bladder epithelial cells.
G. Ding (1991)
10.1126/SCIENCE.279.5350.509
Rho GTPases and the actin cytoskeleton.
A. Hall (1998)
Signaling to the actin cytoskele
A. Schmidt (1998)
10.1073/PNAS.76.12.6376
Reorganization of actin in platelets stimulated by thrombin as measured by the DNase I inhibition assay.
L. Carlsson (1979)
Guidebook to the Cytoskeletal and Motor Proteins, 2nd ed
T. Kreis (1999)
10.1105/tpc.10.6.967
A Potential Signaling Role for Profilin in Pollen of Papaver rhoeas
S. R. Clarke (1998)
10.1046/J.1365-313X.1997.11030525.X
Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non‐host resistance in barley coleoptile cells
Y. Kobayashi (1997)
Reorganization of filamentous actin and myosin-II in zebrafish eggs correlates temporally and spatially with cortical granule exocytosis.
K. A. Becker (1999)
10.1105/tpc.9.11.1999
Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx Is Delayed.
T. Holdaway-Clarke (1997)
10.1046/J.1365-313X.2000.00811.X
Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas.
N. D. Jordan (2000)
10.1104/PP.123.2.645
Calcium-calmodulin suppresses the filamentous actin-binding activity of a 135-kilodalton actin-bundling protein isolated from lily pollen tubes.
E. Yokota (2000)
10.1094/MPMI.1999.12.9.829
Rhizobium Nod Factors Induce an Increase in Sub-apical Fine Bundles of Actin Filaments in Vicia sativa Root Hairs within Minutes
N. Ruijter (1999)
AtFim 1 is an actin filament crosslinking protein from Arabidopsis thaliana
C. J. Staiger
10.1083/JCB.131.6.1483
Actin filaments in yeast are unstable in the absence of capping protein or fimbrin
T. Karpova (1995)
10.1073/PNAS.91.19.8837
Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase.
J. Estruch (1994)
10.1152/AJPCELL.1996.271.6.C1981
Actin polymerization and depolymerization during apoptosis in HL-60 cells.
M. G. Levee (1996)
F-actin as a functional target for retro-retinoids: a potential role in anhydroretinol-triggered cell death.
I. Korichneva (1999)
10.1046/J.1365-313X.1997.00507.X
Ca2+‐independent phosphorylation of a 68 kDa pollen protein is stimulated by the self‐incompatibility response in Papaver rhoeas
J. Rudd (1997)
10.1105/tpc.12.4.583
Maize Profilin Isoforms Are Functionally Distinct
D. Kovar (2000)
10.1073/PNAS.91.6.2265
Cloning and expression of a distinctive class of self-incompatibility (S) gene from Papaver rhoeas L.
H. C. Foote (1994)
10.1016/S0014-5793(96)01259-8
Profilin is required for the normal timing of actin polymerization in response to thermal stress
J. Yeh (1996)
10.1074/jbc.274.10.6234
Filament Assembly from Profilin-Actin*
I. Gutsche-Perelroizen (1999)
10.1104/pp.115.4.1491
Actin Filaments of Guard Cells Are Reorganized in Response to Light and Abscisic Acid
S. Eun (1997)
10.1046/J.1365-313X.1993.04010163.X
The self‐incompatibility response in Papaver rhoeas is mediated by cytosolic free calcium
V. E. Franklin-Tong (1993)
10.1002/(SICI)1097-0169(1998)39:2<166::AID-CM7>3.0.CO;2-4
Rapid and efficient purification of actin from nonmuscle sources.
D. Schafer (1998)
Mechanism of Ca2+ inhibition of cytoplasmic streaming in lily pollen tubes
T. Kohno (1988)
Actin: A Dynamic Framework for
C J Staiger (2000)
10.1016/S0955-0674(99)00062-9
Control of actin assembly and disassembly at filament ends.
J. A. Cooper (2000)
10.1038/hdy.1978.24
The genetical control of self-incompatibility in Papaver rhoeas
M. J. Lawrence (1978)
10.1093/JXB/ERG001
Signals and targets of the self-incompatibility response in pollen of Papaver rhoeas.
J. Rudd (2003)
10.1007/978-94-015-9460-8_6
Characterization of Native Actin-Binding Proteins from Pollen
E. Yokota (2000)
10.1083/JCB.113.4.757
Ca(2+)-independent F-actin assembly and disassembly during Fc receptor- mediated phagocytosis in mouse macrophages
S. Greenberg (1991)
10.1083/JCB.116.3.695
Phorbol ester-induced actin assembly in neutrophils: role of protein kinase C
G. Downey (1992)
10.1104/PP.116.3.871
Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals
Crdenas (1998)
10.1074/jbc.274.52.36963
Profilin Promotes Barbed-end Actin Filament Assembly without Lowering the Critical Concentration*
F. Kang (1999)
10.1091/MBC.12.8.2534
Actin polymerization is essential for pollen tube growth.
L. Vidali (2001)
10.1038/35048692
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana
The Arabidopsis Genome Initiative (2000)
10.1002/(SICI)1097-0169(1996)34:1<36::AID-CM4>3.0.CO;2-G
Plant profilins rescue the aberrant phenotype of profilin-deficient Dictyostelium cells.
I. Karakesisoglou (1996)
10.1146/ANNUREV.CELLBIO.14.1.305
Signaling to the actin cytoskeleton.
A. Schmidt (1998)
10.1007/978-94-015-9460-8_4
Actin Depolymerizing Factor
D. Kovar (2000)
10.1016/s0960-9822(07)00555-6
Caspases and programmed cell death in the hypersensitive response of plants to pathogens
Olga María del Pozo (1998)
A cytoplasmic The Plant Cell gradient of Ca 2ϩ is correlated with the growth of lily pollen tubes
K S Rathore (1991)
10.1046/J.1365-313X.1995.08020299.X
Recombinant stigmatic self‐incompatibility (S‐) protein elicits a Ca2+ transient in pollen of Papaver rhoeas
V. E. Franklin-Tong (1995)
10.1016/S1360-1385(01)02130-6
Rop GTPase: a master switch of cell polarity development in plants.
Y. Fu (2001)
10.1152/PHYSREV.1998.78.3.763
The cytoskeleton and cell signaling: component localization and mechanical coupling.
P. Janmey (1998)
10.1073/pnas.171104598
cAMP acts as a second messenger in pollen tube growth and reorientation
A. Moutinho (2001)
10.1046/J.1365-2818.2000.00702.X
The cytoskeleton in plant and fungal cell tip growth.
A. Geitmann (2000)
10.1083/JCB.125.4.825
Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin-related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae
S. H. Lillie (1994)
10.1002/CM.970050609
A method for quantifying F-actin in chemotactic peptide activated neutrophils: study of the effect of tBOC peptide.
T. Howard (1985)
10.1046/J.1365-313X.1998.00107.X
Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by a calcium-stimulated protein kinase and is essential for the control of functional activity.
A. Smertenko (1998)
10.1105/tpc.10.10.1723
Identification of Residues in a Hydrophilic Loop of the Papaver rhoeas S Protein That Play a Crucial Role in Recognition of Incompatible Pollen
K. Kakeda (1998)
10.1002/(SICI)1097-0169(1997)36:4<323::AID-CM3>3.0.CO;2-6
Characterization and localization of profilin in pollen grains and tubes of Lilium longiflorum.
L. Vidali (1997)
10.1016/S0167-4889(97)00100-6
Profilins as regulators of actin dynamics.
K. Schlüter (1997)
10.1007/978-94-015-9460-8
Actin: A Dynamic Framework for Multiple Plant Cell Functions
C. Staiger (2000)
10.1002/JCB.240370304
Relationship of pseudopod extension to chemotactic hormone‐induced actin polymerization in amoeboid cells
A. L. Hall (1988)
10.1105/tpc.8.4.713
Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas.
J. Rudd (1996)
10.1146/ANNUREV.ARPLANT.51.1.257
SIGNALING TO THE ACTIN CYTOSKELETON IN PLANTS.
C. Staiger (2000)
10.1111/J.1438-8677.1999.TB00240.X
Signals, Motors, Morphogenesis - the Cytoskeleton in Plant Development*
P. Nick (1999)
A cytoplasmic
K. S. Rathore (1991)
Free Ca 2ϩ gradient in growing pollen tubes of Lilium
Vaso - pressin depolymerizes F - actin in toad bladder epithelial cells
G. P. Downey (1991)
10.1146/ANNUREV.CELLBIO.15.1.185
Proteins of the ADF/cofilin family: essential regulators of actin dynamics.
J. Bamburg (1999)
10.1083/JCB.152.5.1019
ROP Gtpase–Dependent Dynamics of Tip-Localized F-Actin Controls Tip Growth in Pollen Tubes
Ying Fu (2001)
10.1083/JCB.101.3.1078
The kinetics of chemotactic peptide-induced change in F-actin content, F-actin distribution, and the shape of neutrophils
T. Howard (1985)
10.1038/86011
Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse
H. Aizawa (2001)
10.1046/J.1365-313X.2002.01219.X
Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas.
V. E. Franklin-Tong (2002)
Profilin is predominantly associated with monomeric actin in Acanthamoeba.
D. A. Kaiser (1999)
10.1046/J.1365-313X.1997.12061375.X
Ratio‐imaging of Ca2+i in the self‐incompatibility response in pollen tubes of Papaver rhoeas
V. E. Franklin-Tong (1997)
10.1006/PMPP.2001.0359
Caspase inhibitors reduce symptom development and limit bacterial proliferation in susceptible plant tissues
C. Richael (2001)
10.1016/S0014-5793(00)01643-4
The presence and subcellular localization of caspase 3‐like proteinases in plant cells
H. Korthout (2000)
10.1046/J.1365-313X.1999.00358.X
The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug
D. Miller (1999)
Free Ca 2  gradient in growing pollen tubes of Lilium
D. D. Miller (1992)



This paper is referenced by
Identification and visualisation of actin-binding proteins in Arabidopsis thaliana and tobacco BY2 cells
Sitara Thotta Nagesh (2013)
10.1371/journal.pone.0116757
Pb-Induced Avoidance-Like Chloroplast Movements in Fronds of Lemna trisulca L.
S. Samardakiewicz (2015)
10.1073/pnas.0705826104
Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen
Maurice Bosch (2007)
Identification of genes related to self-incompatibility in ryegrass (Lolium perenne L.)
I. V. Daele (2005)
10.1371/journal.ppat.1003290
The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns
Jessica L Henty-Ridilla (2013)
10.1093/PCP/PCI185
Plant villin, lily P-135-ABP, possesses G-actin binding activity and accelerates the polymerization and depolymerization of actin in a Ca2+-sensitive manner.
E. Yokota (2005)
Arabidopsis VILLIN 5 , an Actin Filament Bundling and Severing Protein , Is Necessary for Normal Pollen Tube Growth
H. Zhang (2010)
10.1038/ncomms3285
The unusual dynamics of parasite actin result from isodesmic polymerization
Kristen M. Skillman (2013)
10.1105/tpc.110.081802
BENT UPPERMOST INTERNODE1 Encodes the Class II Formin FH5 Crucial for Actin Organization and Rice Development[W][OA]
Wei-bing Yang (2011)
10.1093/pcp/pcn103
A unique caleosin in oil bodies of lily pollen.
Pei-Luen Jiang (2008)
10.1371/journal.ppat.1003006
Arabidopsis Actin-Depolymerizing Factor-4 Links Pathogen Perception, Defense Activation and Transcription to Cytoskeletal Dynamics
K. Porter (2012)
10.1105/tpc.109.068700
Arabidopsis Formin3 Directs the Formation of Actin Cables and Polarized Growth in Pollen Tubes[W]
J. Ye (2009)
Investigations of self-incompatibility (SI) in perennial ryegrass (Lolium perenne L.)
B. Yang (2009)
10.1105/tpc.107.052621
Class-Specific Interaction of Profilin and ADF Isovariants with Actin in the Regulation of Plant Development[W]
M. Kandasamy (2007)
10.1104/pp.107.101741
A Mitogen-Activated Protein Kinase Signals to Programmed Cell Death Induced by Self-Incompatibility in Papaver Pollen1[OA]
S. Li (2007)
10.1371/journal.pgen.1007789
Arabidopsis class I formins control membrane-originated actin polymerization at pollen tube tips
Yaxian Lan (2018)
10.1111/j.1600-0854.2011.01256.x
Actin is Involved in Pollen Tube Tropism Through Redefining the Spatial Targeting of Secretory Vesicles
Firas Bou Daher (2011)
10.1016/J.TPLANTS.2003.10.008
Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms.
N. Franklin-Tong (2003)
10.1016/J.CBPA.2008.04.361
Signalling to programmed cell death in self-incompatible pollen
Maurice Bosch (2008)
Investigating the targets and mechanisms regulating self incompatibility in Papaver rhoeas pollen
Tamanna Haque (2015)
Jcb: Article
Sepideh Dadgar ()
10.1104/pp.20.00066
Self-Incompatibility Triggers Irreversible Oxidative Modification of Proteins in Incompatible Pollen1[CC-BY]
Tamanna Haque (2020)
10.1104/pp.20.00292
Ectopic Expression of a Self-Incompatibility Module Triggers Growth Arrest and Cell Death in Vegetative Cells1[OPEN]
Zongcheng Lin (2020)
10.1074/jbc.M306670200
Arabidopsis Capping Protein (AtCP) Is a Heterodimer That Regulates Assembly at the Barbed Ends of Actin Filaments*
S. Huang (2003)
10.1105/tpc.105.030908
The Formin Homology 1 Domain Modulates the Actin Nucleation and Bundling Activity of Arabidopsis FORMIN1w⃞
Alphée Michelot (2005)
10.1093/JXB/ERM195
Self-incompatibility in Papaver: signalling to trigger PCD in incompatible pollen.
Maurice Bosch (2008)
10.4161/psb.1.2.2432
Actin Turnover-Mediated Gravity Response in Maize Root Apices
S. Mancuso (2006)
10.1038/s41598-017-06431-5
OsFH15, a class I formin, interacts with microfilaments and microtubules to regulate grain size via affecting cell expansion in rice
T. Sun (2017)
10.1104/pp.15.01506
The Cytoskeleton and Its Regulation by Calcium and Protons
P. Hepler (2016)
10.1016/S0014-5793(03)00710-5
Activation of a putative MAP kinase in pollen is stimulated by the self‐incompatibility (SI) response
J. Rudd (2003)
10.1111/J.1469-8137.2004.01076.X
The role of the actin cytoskeleton in plant cell signaling
B. Drøbak (2004)
10.1016/J.SEMCDB.2006.02.005
Fertilization in plants: is calcium a key player?
Christian Dumas (2006)
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