Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1998 Sep;10(9):1499–1510. doi: 10.1105/tpc.10.9.1499

Relocation of a Ca2+-dependent protein kinase activity during pollen tube reorientation

A Moutinho 1, AJ Trewavas 1, R Malho 1
PMCID: PMC144072  PMID: 9724696

Abstract

Pollen tube reorientation is a dynamic cellular event that is crucial for successful fertilization. We have shown previously that pollen tube orientation is regulated by cytosolic free calcium ([Ca2+]c). In this paper, we studied the activity of a Ca2+-dependent protein kinase during reorientation. The kinase activity was assayed in living cells by using confocal ratio imaging of BODIPY FL bisindolylmaleimide. We found that growing pollen tubes exhibited higher protein kinase activity in the apical region, whereas nongrowing cells showed uniform distribution. Modification of growth direction by diffusion of inhibitors/activators from a micropipette showed the spatial redistribution of kinase activity to predict the new growth orientation. Localized increases in [Ca2+]c induced by photolysis of caged Ca2+ that led to reorientation also increased kinase activity. Molecular and immunological assays suggest that this kinase may show some functional homology with protein kinase C. We suggest that the tip-localized gradient of kinase activity promotes Ca2+-mediated exocytosis and may act to regulate Ca2+ channel activity.

Full Text

The Full Text of this article is available as a PDF (544.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abo-el-Saad M., Wu R. A rice membrane calcium-dependent protein kinase is induced by gibberellin. Plant Physiol. 1995 Jun;108(2):787–793. doi: 10.1104/pp.108.2.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burgoyne R. D., Morgan A. Regulated exocytosis. Biochem J. 1993 Jul 15;293(Pt 2):305–316. doi: 10.1042/bj2930305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chen C. S., Poenie M. New fluorescent probes for protein kinase C. Synthesis, characterization, and application. J Biol Chem. 1993 Jul 25;268(21):15812–15822. [PubMed] [Google Scholar]
  4. Drgonová J., Drgon T., Tanaka K., Kollár R., Chen G. C., Ford R. A., Chan C. S., Takai Y., Cabib E. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science. 1996 Apr 12;272(5259):277–279. doi: 10.1126/science.272.5259.277. [DOI] [PubMed] [Google Scholar]
  5. Estruch J. J., Kadwell S., Merlin E., Crossland L. Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8837–8841. doi: 10.1073/pnas.91.19.8837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Holdaway-Clarke T. L., Feijo J. A., Hackett G. R., Kunkel J. G., Hepler P. K. Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx Is Delayed. Plant Cell. 1997 Nov;9(11):1999–2010. doi: 10.1105/tpc.9.11.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ito M., Tanaka T., Inagaki M., Nakanishi K., Hidaka H. N-(6-phenylhexyl)-5-chloro-1-naphthalenesulfonamide, a novel activator of protein kinase C. Biochemistry. 1986 Jul 29;25(15):4179–4184. doi: 10.1021/bi00363a002. [DOI] [PubMed] [Google Scholar]
  8. Kissmehl R., Treptau T., Hofer H. W., Plattner H. Protein phosphatase and kinase activities possibly involved in exocytosis regulation in Paramecium tetraurelia. Biochem J. 1996 Jul 1;317(Pt 1):65–76. doi: 10.1042/bj3170065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Lin Y., Wang Y., Zhu J. K., Yang Z. Localization of a Rho GTPase Implies a Role in Tip Growth and Movement of the Generative Cell in Pollen Tubes. Plant Cell. 1996 Feb;8(2):293–303. doi: 10.1105/tpc.8.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lin Y., Yang Z. Inhibition of Pollen Tube Elongation by Microinjected Anti-Rop1Ps Antibodies Suggests a Crucial Role for Rho-Type GTPases in the Control of Tip Growth. Plant Cell. 1997 Sep;9(9):1647–1659. doi: 10.1105/tpc.9.9.1647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lino B., Baizabal-Aguirre V. M., González de la Vara L. E. The plasma-membrane H(+)-ATPase from beet root is inhibited by a calcium-dependent phosphorylation. Planta. 1998 Mar;204(3):352–359. doi: 10.1007/s004250050266. [DOI] [PubMed] [Google Scholar]
  12. Lu Y. T., Hidaka H., Feldman L. J. Characterization of a calcium/calmodulin-dependent protein kinase homolog from maize roots showing light-regulated gravitropism. Planta. 1996;199(1):18–24. doi: 10.1007/BF00196876. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Malho R., Trewavas A. J. Localized Apical Increases of Cytosolic Free Calcium Control Pollen Tube Orientation. Plant Cell. 1996 Nov;8(11):1935–1949. doi: 10.1105/tpc.8.11.1935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Messerli M., Robinson K. R. Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum. J Cell Sci. 1997 Jun;110(Pt 11):1269–1278. doi: 10.1242/jcs.110.11.1269. [DOI] [PubMed] [Google Scholar]
  16. Muschietti J., Eyal Y., McCormick S. Pollen tube localization implies a role in pollen-pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell. 1998 Mar;10(3):319–330. doi: 10.1105/tpc.10.3.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nanmori T., Taguchi W., Kinugasa M., Oji Y., Sahara S., Fukami Y., Kikkawa U. Purification and characterization of protein kinase C from a higher plant, Brassica campestris L. Biochem Biophys Res Commun. 1994 Aug 30;203(1):311–318. doi: 10.1006/bbrc.1994.2183. [DOI] [PubMed] [Google Scholar]
  18. Nuccitelli R., Smart T., Ferguson J. Protein kinases are required for embryonic neural crest cell galvanotaxis. Cell Motil Cytoskeleton. 1993;24(1):54–66. doi: 10.1002/cm.970240107. [DOI] [PubMed] [Google Scholar]
  19. Olds J. L., Favit A., Nelson T., Ascoli G., Gerstein A., Cameron M., Cameron L., Lester D. S., Rakow T., De Barry J. Imaging protein kinase C activation in living sea urchin eggs after fertilization. Dev Biol. 1995 Dec;172(2):675–682. doi: 10.1006/dbio.1995.8060. [DOI] [PubMed] [Google Scholar]
  20. Petersen C. C., Berridge M. J. The regulation of capacitative calcium entry by calcium and protein kinase C in Xenopus oocytes. J Biol Chem. 1994 Dec 23;269(51):32246–32253. [PubMed] [Google Scholar]
  21. Polya G. M., Micucci V. Interaction of wheat germ ca-dependent protein kinases with calmodulin antagonists and polyamines. Plant Physiol. 1985 Dec;79(4):968–972. doi: 10.1104/pp.79.4.968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ritchie S, Gilroy S. Calcium-Dependent Protein Phosphorylation May Mediate the Gibberellic Acid Response in Barley Aleurone. Plant Physiol. 1998 Feb 1;116(2):765–776. doi: 10.1104/pp.116.2.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schaller G. E., Harmon A. C., Sussman M. R. Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat. Biochemistry. 1992 Feb 18;31(6):1721–1727. doi: 10.1021/bi00121a020. [DOI] [PubMed] [Google Scholar]
  24. Schumaker K. S., Sze H. Inositol 1,4,5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots. J Biol Chem. 1987 Mar 25;262(9):3944–3946. [PubMed] [Google Scholar]
  25. Simpson A. W., Hallam T. J., Rink T. J. TMB-8 inhibits secretion evoked by phorbol ester at basal cytoplasmic free calcium in quin2-loaded platelets much more effectively than it inhibits thrombin-induced calcium mobilisation. FEBS Lett. 1984 Oct 15;176(1):139–143. doi: 10.1016/0014-5793(84)80928-x. [DOI] [PubMed] [Google Scholar]
  26. Sokolova M., Prüfer D., Tacke E., Rohde W. The potato leafroll virus 17K movement protein is phosphorylated by a membrane-associated protein kinase from potato with biochemical features of protein kinase C. FEBS Lett. 1997 Jan 3;400(2):201–205. doi: 10.1016/s0014-5793(96)01380-4. [DOI] [PubMed] [Google Scholar]
  27. Subramaniam R., Després C., Brisson N. A functional homolog of mammalian protein kinase C participates in the elicitor-induced defense response in potato. Plant Cell. 1997 Apr;9(4):653–664. doi: 10.1105/tpc.9.4.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Thomas A. P., Bird G. S., Hajnóczky G., Robb-Gaspers L. D., Putney J. W., Jr Spatial and temporal aspects of cellular calcium signaling. FASEB J. 1996 Nov;10(13):1505–1517. [PubMed] [Google Scholar]
  29. Toullec D., Pianetti P., Coste H., Bellevergue P., Grand-Perret T., Ajakane M., Baudet V., Boissin P., Boursier E., Loriolle F. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem. 1991 Aug 25;266(24):15771–15781. [PubMed] [Google Scholar]
  30. Trewavas A. J., Malho R. Signal Perception and Transduction: The Origin of the Phenotype. Plant Cell. 1997 Jul;9(7):1181–1195. doi: 10.1105/tpc.9.7.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Trotter P. J., Orchard M. A., Walker J. H. Ca2+ concentration during binding determines the manner in which annexin V binds to membranes. Biochem J. 1995 Jun 1;308(Pt 2):591–598. doi: 10.1042/bj3080591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Verhey S. D., Gaiser J. C., Lomax T. L. Protein Kinases in Zucchini (Characterization of Calcium-Requiring Plasma Membrane Kinases). Plant Physiol. 1993 Oct;103(2):413–419. doi: 10.1104/pp.103.2.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van der Hoeven P. C., Siderius M., Korthout H. A., Drabkin A. V., de Boer A. H. A calcium and free fatty acid-modulated protein kinase as putative effector of the fusicoccin 14-3-3 receptor. Plant Physiol. 1996 Jul;111(3):857–865. doi: 10.1104/pp.111.3.857. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES