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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, B. Drøbak, A. Allan, P. Watkins, A. Trewavas
Published 1996 · Chemistry, Biology, Medicine

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A signaling role for cytosolic free Ca2+ ([Ca2+]i) in regulating Papaver rhoeas pollen tube growth during the self-incompatibility response has been demonstrated previously. In this article, we investigate the involvement of the phosphoinositide signal transduction pathway in Ca2+-mediated pollen tube inhibition. We demonstrate that P. rhoeas pollen tubes have a Ca2+-dependent polyphosphoinositide-specific phospholipase C activity that is inhibited by neomycin. [Ca2+]i imaging after photolysis of caged inositol (1,4,5)-trisphosphate (Ins[1,4,5]P3) in pollen tubes demonstrated that Ins(1,4,5)P3 could induce Ca2+ release, which was inhibited by heparin and neomycin. Mastoparan, which stimulated Ins(1,4,5)P3 production, also induced a rapid increase in Ca2+, which was inhibited by neomycin. These data provide direct evidence for the involvement of a functional phosphoinositide signal-transducing system in the regulation of pollen tube growth. We suggest that the observed Ca2+ increases are mediated, at least in part, by Ins(1,4,5)P3-induced Ca2+ release. Furthermore, we provide data suggesting that Ca2+ waves, which have not previously been reported in plant cells, can be induced in pollen tubes.
This paper references
10.1006/DBIO.1995.0011
Effect on sperm-induced activation current and increase of cytosolic Ca2+ by agents that modify the mobilization of [Ca2+]i. I. Heparin and pentosan polysulfate.
T. Mohri (1995)
10.1016/0031-9422(86)80065-6
Phosphatidylinositol phospholipase C activity in pollen of Lilium longiflorum
J. P. F. G. Helsper (1986)
10.1016/0168-9452(93)90233-P
Is vacuole the richest store of IP3-mobilizable calcium in plant cells?
H. Canut (1993)
10.1111/J.1365-313X.1994.00331.X
Role of cytosolic free calcium in the reorientation of pollen tube growth
R. Malhó (1994)
10.1038/360076A0
Calcium-dependent immediate feedback control of inositol 1,4,5-trisphosphate-induced Ca2+ release
M. Iino (1992)
10.1105/tpc.6.5.685
Two Voltage-Gated, Calcium Release Channels Coreside in the Vacuolar Membrane of Broad Bean Guard Cells.
G. Allen (1994)
10.1016/0163-7827(92)90015-B
Inositol-containing lipids in higher plants.
A. Hetherington (1992)
Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells.
L. Legendre (1993)
10.1038/346769A0
Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure
S. Gilroy (1990)
Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes.
G. Obermeyer (1991)
Free Ca2+ Gradient in Growing Pollen Tubes of Lillium
D. Miller (1992)
10.1073/PNAS.92.9.3903
A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana.
T. Hirayama (1995)
10.1038/361315A0
Inositol trisphosphate and calcium signalling
M. Berridge (1993)
10.1111/J.1469-8137.1988.TB00243.X
An in vitro bioassay for the stigmatic product of the self‐incompatibility gene in Papaver rhoeas L.
V. E. Franklin-Tong (1988)
Competitive, reversible, and potent antagonism of inositol 1,4,5-trisphosphate-activated calcium release by heparin.
T. K. Ghosh (1988)
10.1104/pp.107.3.845
The Effects of Mastoparan on the Carrot Cell Plasma Membrane Polyphosphoinositide Phospholipase C
M. H. Cho (1995)
10.1105/tpc.4.10.1180
Excitation in Plant Membrane Biology
R. Chasan (1992)
10.1085/JGP.97.4.697
The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors
T. Frank (1991)
10.1083/JCB.67.2.488
Calcium accumulations within the growing tips of pollen tubes
L. Jaffe (1975)
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)
10.1016/0014-5793(90)80068-T
Inositol trisphosphate‐mediated Ca2+ release in beet mu;somes is inhibited by heparin
J. M. Brosnan (1990)
10.1105/tpc.5.8.931
Identification and Characterization of High-Affinity Binding Sites for Inositol Trisphosphate in Red Beet.
J. M. Brosnan (1993)
10.1016/0014-5793(86)80343-X
Neomycin: a specific drug to study the inositol‐phospholipid signalling system?
M. Prentki (1986)
10.1038/377438A0
Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes
L. Jouaville (1995)
10.1038/326301A0
Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes
M. Kuno (1987)
10.1006/BBRC.1993.2604
The inhibition of the inositol 1,4,5-trisphosphate receptor from rat cerebellum by spermine and other polyamines.
L. Sayers (1993)
10.1074/JBC.271.14.8387
Interaction between Ryanodine and Neomycin Binding Sites on Ca Release Channel from Skeletal Muscle Sarcoplasmic Reticulum (*)
J. Wang (1996)
Nifedipine-sensitive calcium channels are involved in polar growth of lily pollen tubes.
H. Reiss (1985)
10.1016/0006-291X(85)91747-4
Release of Ca2+ from plant hypocotyl microsomes by inositol-1,4,5-trisphosphate.
B. Drøbak (1985)
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)
10.1016/0005-2760(92)90107-7
Polyphosphoinositide phospholipase C in wheat root plasma membranes. Partial purification and characterization.
P. Melin (1992)
10.1016/S0006-291X(88)81141-0
Heparin inhibits the inositol 1,4,5-trisphosphate-dependent, but not the independent, calcium release induced by guanine nucleotide in vascular smooth muscle.
S. Kobayashi (1988)
10.1146/ANNUREV.PP.46.060195.000523
Calcium Regulation in Plant Cells and its Role in Signaling
D. Bush (1995)
10.1042/BJ2880697
The plant phosphoinositide system.
B. Drøbak (1992)
10.1002/CM.970280402
Signal transduction and calcium: a suggested role for the cytoskeleton in inositol 1,4,5-trisphosphate action.
N. Kraus-Friedmann (1994)
Cortical endoplasmic reticulum in plants
P. K. Hepler (1990)
10.1002/J.1537-2197.1963.TB06564.X
THE ESSENTIAL ROLE OF CALCIUM ION IN POLLEN GERMINATION AND POLLEN TUBE GROWTH
J. Brewbaker (1963)
10.1016/0168-9525(91)90255-O
Signal transduction in plant cells.
A. Trewavas (1991)
10.1016/0012-1606(91)90278-B
A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes.
K. Rathore (1991)
10.1104/PP.96.1.340
Neomycin inhibits the phosphatidylinositol monophosphate and phosphatidylinositol bisphosphate stimulation of plasma membrane ATPase activity.
Q. Chen (1991)
10.1104/PP.95.2.412
Metabolism of Inositol(1,4,5)trisphosphate by a Soluble Enzyme Fraction from Pea (Pisum sativum) Roots.
B. Drøbak (1991)
10.1016/0143-4160(93)90099-R
Classes and mechanisms of calcium waves.
L. Jaffe (1993)
Inositol 1,4,5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots.
K. Schumaker (1987)
10.1105/tpc.6.9.1319
Two Transduction Pathways Mediate Rapid Effects of Abscisic Acid in Commelina Guard Cells.
A. Allan (1994)
10.1105/tpc.6.12.1815
Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media.
Elisabeth S. Pierson (1994)
10.1105/tpc.7.8.1173
Calcium Channel Activity during Pollen Tube Growth and Reorientation.
R. Malhó (1995)
10.1046/J.1365-313X.1994.06030389.X
Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin‐binding protein, profilin
B. Drøbak (1994)
Effects of the amphiphilic peptides melittin and mastoparan on calcium influx, phosphoinositide breakdown and arachidonic acid release in rat pheochromocytoma PC12 cells.
O. H. Choi (1992)
10.1105/tpc.7.8.1207
Stimulus-Induced Oscillations in Guard Cell Cytosolic Free Calcium.
M. McAinsh (1995)
10.1105/tpc.4.9.1113
Visualizing Changes in Cytosolic-Free Ca2+ during the Response of Stomatal Guard Cells to Abscisic Acid.
M. McAinsh (1992)
10.1111/J.1469-8137.1989.TB00697.X
Pollen tube tip growth
M. Steer (1989)
10.1042/BJ3060631
Receptor for myo-inositol trisphosphate from the microsomal fraction of Vigna radiata.
S. Biswas (1995)
10.1083/JCB.116.3.737
Inositol phospholipid metabolism may trigger flagellar excision in Chlamydomonas reinhardtii
L. Quarmby (1992)
10.1038/358753A0
Cytosolic free calcium mediates red light-induced photomorphogenesis
P. Shacklock (1992)
10.1146/ANNUREV.PP.44.060193.002001
Biochemistry of Phosphoinositides
G. G. Coté (1993)
10.1111/J.1399-3054.1987.TB04628.X
Cytosolic and particulate phosphatidylinositol phospholipase C activities in pollen tubes of Lilium longiflorum
J. P. F. G. Helsper (1987)
10.1083/JCB.76.2.448
A free calcium wave traverses the activating egg of the medaka, Oryzias latipes
J. C. Gilkey (1978)
10.1007/BF00205228
Dynamic aspects of apical zonation in the angiosperm pollen tube
J. Heslop-Harrison (2004)
Calcium homeostasis in plants.
S. Gilroy (1993)
10.1046/J.1365-313X.1995.08020257.X
Multiple phosphoinositide‐specific phospholipases C in oat roots: characterization and partial purification
Chiung-Hua Huang (1995)
10.1016/0005-2760(89)90018-0
Effects of the wasp venom peptide, mastoparan, on a phosphoinositide-specific phospholipase C purified from rabbit brain membranes.
M. Wallace (1989)



This paper is referenced by
10.1073/PNAS.95.5.2697
Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity.
S. Ritchie (1998)
10.1104/PP.126.1.39
Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength?
F. Baluška (2001)
Fluctuation of cytosolic calcium in maize guard cell pairs induced by ABA
Liu Zi-hui (2008)
10.1016/S1369-5266(00)00194-1
Calcium oscillations in higher plants.
N. H. Evans (2001)
Identification and Functional Role of Myo-Inositol Polyphosphate 5-Phosphatase Protein Complexes
E. Ananieva-Stoyanova (2009)
10.1042/BST0240971
Transduction of Ca2+ signals in plant cells and compartmentalization of the Ca2+ signal.
A. Trewavas (1996)
10.1105/TPC.001115
Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants.
S. Luan (2002)
10.1093/JXB/ERM195
Self-incompatibility in Papaver: signalling to trigger PCD in incompatible pollen.
Maurice Bosch (2008)
10.1007/s11515-011-1110-1
Actin organization and regulation during pollen tube growth
Xiuhua Xue (2011)
10.1016/S0014-5793(99)01109-6
Calcium‐induced calcium release mediated by a voltage‐activated cation channel in vacuolar vesicles from red beet
M. A. Bewell (1999)
10.1093/TREEPHYS/23.5.345
Boron influences pollen germination and pollen tube growth in Picea meyeri.
Qinli Wang (2003)
Pollen Tube Growt h and the lntracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx 1 s Delayed
T. Holdaway-Clarke (2007)
10.1078/0176-1617-00550
Calcium-mediated signal transduction in plants : A perspective on the role of Ca2+ and CDPKs during early plant development
V. S. Anil (2001)
10.1078/0176-1617-00834
Abscisic acid signaling and protein synthesis requirements for phosphoenolpyruvate carboxylase transcript induction in the common ice plant
T. Taybi (2002)
10.1093/PCP/PCE111
Structure and function of heterotrimeric G proteins in plants.
Y. Fujisawa (2001)
Spikes and Waves : Calcium-Mediated Signaling in Ti p-Grow i ng Cel 1 s
()
10.1016/S0300-9084(99)80124-2
Recent advances in the study of nod factor perception and signal transduction.
A. Niebel (1999)
10.1104/PP.118.3.759
Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells
Subbaiah (1998)
10.1093/PCP/41.4.399
Possible involvement of phosphoinositide-Ca2+ signaling in the regulation of alpha-amylase expression and germination of rice seed (Oryza sativa L.).
M. A. Kashem (2000)
10.1093/PCP/PCH020
Cryptogein-induced initial events in tobacco BY-2 cells: pharmacological characterization of molecular relationship among cytosolic Ca(2+) transients, anion efflux and production of reactive oxygen species.
Yasuhiro Kadota (2004)
LipidMetabolism, Compartmentalization and Signalling in the Regulation of Pollen Tube Growth
V. Žárský (2006)
10.1104/pp.103.029454
Osmotically Induced Cell Swelling versus Cell Shrinking Elicits Specific Changes in Phospholipid Signals in Tobacco Pollen Tubes1
L. Zonia (2004)
10.1046/J.1365-313X.2000.00819.X
An increase in phosphoinositide-specific phospholipase C activity precedes induction of C4 phosphoenolpyruvate carboxylase phosphorylation in illuminated and NH4Cl-treated protoplasts from Digitaria sanguinalis.
S. Coursol (2000)
10.1104/pp.107.113035
Pollen Tube Growth Oscillations and Intracellular Calcium Levels Are Reversibly Modulated by Actin Polymerization1[OA]
L. Cárdenas (2008)
10.1073/PNAS.020516397
Elemental propagation of calcium signals in response-specific patterns determined by environmental stimulus strength.
H. Goddard (2000)
10.1073/PNAS.96.10.5838
Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini.
I. Perera (1999)
10.1562/2006-03-08-IR-837
Phototropins and Blue Light‐dependent Calcium Signaling in Higher Plants †
A. Harada (2007)
10.1038/nature02540
Self-incompatibility triggers programmed cell death in Papaver pollen
S. Thomas (2004)
10.1104/pp.104.045427
A Role of Arabidopsis Inositol Polyphosphate Kinase, AtIPK2α, in Pollen Germination and Root Growth1
Jun Xu (2005)
Investigating the targets and mechanisms regulating self incompatibility in Papaver rhoeas pollen
Tamanna Haque (2015)
10.1105/tpc.005702
A Tumor Suppressor Homolog, AtPTEN1, Is Essential for Pollen Development in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.005702.
R. Gupta (2002)
10.1105/tpc.8.11.1915
Spikes and Waves: Calcium-Mediated Signaling in Tip-Growing Cells
K. Schumaker (1996)
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