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. 1996 Nov;8(11):1935–1949. doi: 10.1105/tpc.8.11.1935

Localized Apical Increases of Cytosolic Free Calcium Control Pollen Tube Orientation.

R Malho 1, A J Trewavas 1
PMCID: PMC161325  PMID: 12239370

Abstract

To reach the ovule, pollen tubes must undergo many changes in growth direction. We have shown in previous work that elevation of cytosolic free calcium ([Ca2+]c) can manipulate orientation in growing pollen tubes, but our results suggested that [Ca2+]c changes either in the tip or in more distal regions might regulate the critical orienting mechanism. To identify the spatial location of the orienting motor, we combined the techniques of ion imaging with confocal microscopy and localized photoactivation of loaded caged Ca2+ (nitr-5) and diazo-2 (a caged Ca2+ chelator) to manipulate [Ca2+]c in different pollen tube domains. We found that increasing [Ca2+]c on one side of the pollen tube apex induced reorientation of the growth axis toward that side. Similarly, a decrease in [Ca2+]c promoted bending toward the opposite side. These effects could be mimicked by imposing localized external gradients of an ionophore (A23187) or a Ca2+ channel blocker (GdCl3); the pollen tubes bend toward the highest concentration of A23187 and away from GdCl3. Manipulation of [Ca2+]c in regions farther back from the apical zone also induced changes in growth direction, but the new orientation was at random. We observed communication of these distal events to the tip through a slow-moving [Ca2+]c wave. These data show that localized changes of [Ca2+]c in the tip, which could result from asymmetric channel activity, control the direction of pollen tube growth.

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Selected References

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  1. 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]
  2. Björkman T., Cleland R. E. The role of extracellular free-calcium gradients in gravitropic signalling in maize roots. Planta. 1991;185:379–384. [PubMed] [Google Scholar]
  3. Blackbourn H. D., Barker P. J., Huskisson N. S., Battey N. H. Properties and partial protein sequence of plant annexins. Plant Physiol. 1992 Jul;99(3):864–871. doi: 10.1104/pp.99.3.864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bootman M. D., Berridge M. J. The elemental principles of calcium signaling. Cell. 1995 Dec 1;83(5):675–678. doi: 10.1016/0092-8674(95)90179-5. [DOI] [PubMed] [Google Scholar]
  5. Bouget F. Y., Gerttula S., Shaw S. L., Quatrano R. S. Localization of Actin mRNA during the Establishment of Cell Polarity and Early Cell Divisions in Fucus Embryos. Plant Cell. 1996 Feb;8(2):189–201. doi: 10.1105/tpc.8.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown E. M., Vassilev P. M., Hebert S. C. Calcium ions as extracellular messengers. Cell. 1995 Dec 1;83(5):679–682. doi: 10.1016/0092-8674(95)90180-9. [DOI] [PubMed] [Google Scholar]
  7. Cheung A. Y., Wang H., Wu H. M. A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell. 1995 Aug 11;82(3):383–393. doi: 10.1016/0092-8674(95)90427-1. [DOI] [PubMed] [Google Scholar]
  8. Ding J. P., Pickard B. G. Mechanosensory calcium-selective cation channels in epidermal cells. Plant J. 1993;3(1):83–110. doi: 10.1111/j.1365-313x.1993.tb00013.x. [DOI] [PubMed] [Google Scholar]
  9. Franklin-Tong V. E., Drobak B. K., Allan A. C., Watkins PAC., Trewavas A. J. Growth of Pollen Tubes of Papaver rhoeas Is Regulated by a Slow-Moving Calcium Wave Propagated by Inositol 1,4,5-Trisphosphate. Plant Cell. 1996 Aug;8(8):1305–1321. doi: 10.1105/tpc.8.8.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Goodner B., Quatrano R. S. Fucus Embryogenesis: A Model to Study the Establishment of Polarity. Plant Cell. 1993 Oct;5(10):1471–1481. doi: 10.1105/tpc.5.10.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Huang J. W., Grunes D. L., Kochian L. V. Voltage-dependent Ca2+ influx into right-side-out plasma membrane vesicles isolated from wheat roots: characterization of a putative Ca2+ channel. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3473–3477. doi: 10.1073/pnas.91.8.3473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hulskamp M., Schneitz K., Pruitt R. E. Genetic Evidence for a Long-Range Activity That Directs Pollen Tube Guidance in Arabidopsis. Plant Cell. 1995 Jan;7(1):57–64. doi: 10.1105/tpc.7.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Johnson C. H., Knight M. R., Kondo T., Masson P., Sedbrook J., Haley A., Trewavas A. Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science. 1995 Sep 29;269(5232):1863–1865. doi: 10.1126/science.7569925. [DOI] [PubMed] [Google Scholar]
  16. Kao J. P., Harootunian A. T., Tsien R. Y. Photochemically generated cytosolic calcium pulses and their detection by fluo-3. J Biol Chem. 1989 May 15;264(14):8179–8184. [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Mascarenhas J. P., Machlis L. Chemotropic Response of the Pollen of Antirrhinum majus to Calcium. Plant Physiol. 1964 Jan;39(1):70–77. doi: 10.1104/pp.39.1.70. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. Pierson E. S., Miller D. D., Callaham D. A., van Aken J., Hackett G., Hepler P. K. Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol. 1996 Feb 25;174(1):160–173. doi: 10.1006/dbio.1996.0060. [DOI] [PubMed] [Google Scholar]
  24. Rapp G., Güth K. A low cost high intensity flash device for photolysis experiments. Pflugers Arch. 1988 Feb;411(2):200–203. doi: 10.1007/BF00582315. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Rizzuto R., Brini M., Murgia M., Pozzan T. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science. 1993 Oct 29;262(5134):744–747. doi: 10.1126/science.8235595. [DOI] [PubMed] [Google Scholar]
  27. Rubinstein A. L., Marquez J., Suarez-Cervera M., Bedinger P. A. Extensin-like Glycoproteins in the Maize Pollen Tube Wall. Plant Cell. 1995 Dec;7(12):2211–2225. doi: 10.1105/tpc.7.12.2211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schiefelbein J., Galway M., Masucci J., Ford S. Pollen tube and root-hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol. 1993 Nov;103(3):979–985. doi: 10.1104/pp.103.3.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thuleau P., Moreau M., Schroeder J. I., Ranjeva R. Recruitment of plasma membrane voltage-dependent calcium-permeable channels in carrot cells. EMBO J. 1994 Dec 15;13(24):5843–5847. doi: 10.1002/j.1460-2075.1994.tb06928.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Thuleau P., Ward J. M., Ranjeva R., Schroeder J. I. Voltage-dependent calcium-permeable channels in the plasma membrane of a higher plant cell. EMBO J. 1994 Jul 1;13(13):2970–2975. doi: 10.1002/j.1460-2075.1994.tb06595.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wu H. M., Wang H., Cheung A. Y. A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell. 1995 Aug 11;82(3):395–403. doi: 10.1016/0092-8674(95)90428-x. [DOI] [PubMed] [Google Scholar]

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