Abstract
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.
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- Allan A. C., Fricker M. D., Ward J. L., Beale M. H., Trewavas A. J. Two Transduction Pathways Mediate Rapid Effects of Abscisic Acid in Commelina Guard Cells. Plant Cell. 1994 Sep;6(9):1319–1328. doi: 10.1105/tpc.6.9.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Allen G. J., Sanders D. Two Voltage-Gated, Calcium Release Channels Coreside in the Vacuolar Membrane of Broad Bean Guard Cells. Plant Cell. 1994 May;6(5):685–694. doi: 10.1105/tpc.6.5.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
- Biswas S., Dalal B., Sen M., Biswas B. B. Receptor for myo-inositol trisphosphate from the microsomal fraction of Vigna radiata. Biochem J. 1995 Mar 15;306(Pt 3):631–636. doi: 10.1042/bj3060631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blatt M. R., Thiel G., Trentham D. R. Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate. Nature. 1990 Aug 23;346(6286):766–769. doi: 10.1038/346766a0. [DOI] [PubMed] [Google Scholar]
- Brosnan J. M., Sanders D. Identification and Characterization of High-Affinity Binding Sites for Inositol Trisphosphate in Red Beet. Plant Cell. 1993 Aug;5(8):931–940. doi: 10.1105/tpc.5.8.931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cho M. H., Tan Z., Erneux C., Shears S. B., Boss W. F. The effects of mastoparan on the carrot cell plasma membrane polyphosphoinositide phospholipase C. Plant Physiol. 1995 Mar;107(3):845–856. doi: 10.1104/pp.107.3.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drøbak B. K., Ferguson I. B. Release of Ca2+ from plant hypocotyl microsomes by inositol-1,4,5-trisphosphate. Biochem Biophys Res Commun. 1985 Aug 15;130(3):1241–1246. doi: 10.1016/0006-291x(85)91747-4. [DOI] [PubMed] [Google Scholar]
- Drøbak B. K., Watkins P. A., Chattaway J. A., Roberts K., Dawson A. P. Metabolism of Inositol(1,4,5)trisphosphate by a Soluble Enzyme Fraction from Pea (Pisum sativum) Roots. Plant Physiol. 1991 Feb;95(2):412–419. doi: 10.1104/pp.95.2.412. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frank T. M., Fein A. The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors. J Gen Physiol. 1991 Apr;97(4):697–723. doi: 10.1085/jgp.97.4.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ghosh T. K., Eis P. S., Mullaney J. M., Ebert C. L., Gill D. L. Competitive, reversible, and potent antagonism of inositol 1,4,5-trisphosphate-activated calcium release by heparin. J Biol Chem. 1988 Aug 15;263(23):11075–11079. [PubMed] [Google Scholar]
- Gilkey J. C., Jaffe L. F., Ridgway E. B., Reynolds G. T. A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J Cell Biol. 1978 Feb;76(2):448–466. doi: 10.1083/jcb.76.2.448. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilroy S., Bethke P. C., Jones R. L. Calcium homeostasis in plants. J Cell Sci. 1993 Oct;106(Pt 2):453–461. doi: 10.1242/jcs.106.2.453. [DOI] [PubMed] [Google Scholar]
- Gilroy S., Read N. D., Trewavas A. J. Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature. 1990 Aug 23;346(6286):769–771. doi: 10.1038/346769a0. [DOI] [PubMed] [Google Scholar]
- Hetherington A. M., Drøbak B. K. Inositol-containing lipids in higher plants. Prog Lipid Res. 1992;31(1):53–63. doi: 10.1016/0163-7827(92)90015-b. [DOI] [PubMed] [Google Scholar]
- Hirayama T., Ohto C., Mizoguchi T., Shinozaki K. A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3903–3907. doi: 10.1073/pnas.92.9.3903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jaffe L. F. Classes and mechanisms of calcium waves. Cell Calcium. 1993 Nov;14(10):736–745. doi: 10.1016/0143-4160(93)90099-r. [DOI] [PubMed] [Google Scholar]
- Joseph S. K., Esch T., Bonner W. D., Jr Hydrolysis of inositol phosphates by plant cell extracts. Biochem J. 1989 Dec 15;264(3):851–856. doi: 10.1042/bj2640851. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jouaville L. S., Ichas F., Holmuhamedov E. L., Camacho P., Lechleiter J. D. Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature. 1995 Oct 5;377(6548):438–441. doi: 10.1038/377438a0. [DOI] [PubMed] [Google Scholar]
- Kobayashi S., Somlyo A. V., Somlyo A. P. Heparin inhibits the inositol 1,4,5-trisphosphate-dependent, but not the independent, calcium release induced by guanine nucleotide in vascular smooth muscle. Biochem Biophys Res Commun. 1988 Jun 16;153(2):625–631. doi: 10.1016/s0006-291x(88)81141-0. [DOI] [PubMed] [Google Scholar]
- Kraus-Friedmann N. Signal transduction and calcium: a suggested role for the cytoskeleton in inositol 1,4,5-trisphosphate action. Cell Motil Cytoskeleton. 1994;28(4):279–284. doi: 10.1002/cm.970280402. [DOI] [PubMed] [Google Scholar]
- Kuno M., Gardner P. Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes. Nature. 1987 Mar 19;326(6110):301–304. doi: 10.1038/326301a0. [DOI] [PubMed] [Google Scholar]
- Legendre L., Yueh Y. G., Crain R., Haddock N., Heinstein P. F., Low P. S. Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells. J Biol Chem. 1993 Nov 25;268(33):24559–24563. [PubMed] [Google Scholar]
- Malho R., Read N. D., Trewavas A. J., Pais M. S. Calcium Channel Activity during Pollen Tube Growth and Reorientation. Plant Cell. 1995 Aug;7(8):1173–1184. doi: 10.1105/tpc.7.8.1173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McAinsh M. R., Brownlee C., Hetherington A. M. Visualizing Changes in Cytosolic-Free Ca2+ during the Response of Stomatal Guard Cells to Abscisic Acid. Plant Cell. 1992 Sep;4(9):1113–1122. doi: 10.1105/tpc.4.9.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McAinsh M. R., Webb AAR., Taylor J. E., Hetherington A. M. Stimulus-Induced Oscillations in Guard Cell Cytosolic Free Calcium. Plant Cell. 1995 Aug;7(8):1207–1219. doi: 10.1105/tpc.7.8.1207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Michelangeli F., Mezna M., Tovey S., Sayers L. G. Pharmacological modulators of the inositol 1,4,5-trisphosphate receptor. Neuropharmacology. 1995 Sep;34(9):1111–1122. doi: 10.1016/0028-3908(95)00053-9. [DOI] [PubMed] [Google Scholar]
- Miyazaki S., Yuzaki M., Nakada K., Shirakawa H., Nakanishi S., Nakade S., Mikoshiba K. Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science. 1992 Jul 10;257(5067):251–255. doi: 10.1126/science.1321497. [DOI] [PubMed] [Google Scholar]
- Mohri T., Ivonnet P. I., Chambers E. L. 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. Dev Biol. 1995 Nov;172(1):139–157. doi: 10.1006/dbio.1995.0011. [DOI] [PubMed] [Google Scholar]
- Obermeyer G., Weisenseel M. H. Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol. 1991 Dec;56(2):319–327. [PubMed] [Google Scholar]
- Pierson E. S., Miller D. D., Callaham D. A., Shipley A. M., Rivers B. A., Cresti M., Hepler P. K. Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell. 1994 Dec;6(12):1815–1828. doi: 10.1105/tpc.6.12.1815. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prentki M., Deeney J. T., Matschinsky F. M., Joseph S. K. Neomycin: a specific drug to study the inositol-phospholipid signalling system? FEBS Lett. 1986 Mar 3;197(1-2):285–288. doi: 10.1016/0014-5793(86)80343-x. [DOI] [PubMed] [Google Scholar]
- Quarmby L. M., Yueh Y. G., Cheshire J. L., Keller L. R., Snell W. J., Crain R. C. Inositol phospholipid metabolism may trigger flagellar excision in Chlamydomonas reinhardtii. J Cell Biol. 1992 Feb;116(3):737–744. doi: 10.1083/jcb.116.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rathore K. S., Cork R. J., Robinson K. R. A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Dev Biol. 1991 Dec;148(2):612–619. doi: 10.1016/0012-1606(91)90278-b. [DOI] [PubMed] [Google Scholar]
- Reiss H. D., Herth W. Nifedipine-sensitive calcium channels are involved in polar growth of lily pollen tubes. J Cell Sci. 1985 Jun;76:247–254. doi: 10.1242/jcs.76.1.247. [DOI] [PubMed] [Google Scholar]
- Rudd J. J., Franklin FCH., Lord J. M., Franklin-Tong V. E. Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas. Plant Cell. 1996 Apr;8(4):713–724. doi: 10.1105/tpc.8.4.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sayers L. G., Michelangeli F. The inhibition of the inositol 1,4,5-trisphosphate receptor from rat cerebellum by spermine and other polyamines. Biochem Biophys Res Commun. 1993 Dec 30;197(3):1203–1208. doi: 10.1006/bbrc.1993.2604. [DOI] [PubMed] [Google Scholar]
- Wallace M. A., Carter H. R. Effects of the wasp venom peptide, mastoparan, on a phosphoinositide-specific phospholipase C purified from rabbit brain membranes. Biochim Biophys Acta. 1989 Dec 18;1006(3):311–316. doi: 10.1016/0005-2760(89)90018-0. [DOI] [PubMed] [Google Scholar]
- Wang J. P., Needleman D. H., Seryshev A. B., Aghdasi B., Slavik K. J., Liu S. Q., Pedersen S. E., Hamilton S. L. Interaction between ryanodine and neomycin binding sites on Ca2+ release channel from skeletal muscle sarcoplasmic reticulum. J Biol Chem. 1996 Apr 5;271(14):8387–8393. doi: 10.1074/jbc.271.14.8387. [DOI] [PubMed] [Google Scholar]
- Worley P. F., Baraban J. M., Supattapone S., Wilson V. S., Snyder S. H. Characterization of inositol trisphosphate receptor binding in brain. Regulation by pH and calcium. J Biol Chem. 1987 Sep 5;262(25):12132–12136. [PubMed] [Google Scholar]