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Endocytosis and Membrane Recycling in Pollen Tubes

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Plant Endocytosis

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 1))

Abstract

In plants, tip-growing cells are an ideal system to investigate signal transduction mechanisms and, among these, pollen tubes are one of the favourite models. Many signalling pathways have been identified during germination and tip growth and, not surprisingly, the apical secretory machinery, essential for tip growth, seems to be an intersection point for all these pathways. Here we review previous data on the pollen tube endocytic machinery and its coupling to the exocytic delivery of new cell wall material. Additionally, we discuss new methodologies and how these are shaping our current working hypothesis to explain endocytosis in pollen tubes.

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References

  1. Ammala C, Ashcroft FM, Rorsman P (1993) Calcium-independent potentiation of insulin release by cyclic AMP in single beta-cells. Nature 363:356–358

    Article  PubMed  Google Scholar 

  2. Artalejo CR, Henley JR, McNiven MA, Palfrey HC (1995) Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP and dynamin but not clathrin. Proc Natl Acad Sci USA 92:8328–8332

    PubMed  Google Scholar 

  3. Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11:643–659

    Article  PubMed  Google Scholar 

  4. Camacho L, Malhó R (2003) Endo-exocytosis in the pollen tube apex is diferentially regulated by Ca2+and GTPases. J Exp Bot 54:83–92

    Article  PubMed  Google Scholar 

  5. Cheung AY, Wu H-M (2004) Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 16:257–269

    Article  PubMed  Google Scholar 

  6. Cremona O, Di Paolo G, Wenk MR, Lüthi A, Kim WT, Takei K, Daniell L, Nemoto Y, Shears SB, Flavell RA, McCormick DA, De Camilli P (1999) Essential role of phophoinositol metabolism in synaptic vesicle recycling. Cell 99:179–188

    Article  PubMed  Google Scholar 

  7. De Graaf BHJ, Derksen JWM, Mariani C (2001) Pollen and pistil in the progamic phase. Sex Plant Reprod 14:41–55

    Article  Google Scholar 

  8. Derksen J, Knuiman B, Hoedemaekers K, Guyon A, Bonhomme S, Pierson ES (2002) Growth and cellular organization of Arabidopsis pollen tubes in vitro. Sex Plant Reprod 15:133–139

    Article  Google Scholar 

  9. Derksen J, Rutten T, Lichtscheidl IK, de Win AHN, Pierson ES, Rongen G (1995) Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis. Protoplasma 188:267–276

    Article  Google Scholar 

  10. Derksen J, Rutten T, van Amstel T, de Win A, Doris F, Steer M (1995a) Regulation of pollen tube growth. Acta Bot Neerl 44:93–119

    Google Scholar 

  11. Derksen J, van Wezel R, Knuiman B, Ylstra B, van Tunen AJ (1999) Pollen tubes of flavonol-deficient Petunia show striking alterations in wall structure leading to tube disruption. Planta 207:575–581

    Article  Google Scholar 

  12. Drøbak BK, Watkins PAC, Valenta R, Dove SK, Lloyd CW, Staiger CJ (1994) Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin-binding protein, profilin. Plant J 6:389–400

    Article  Google Scholar 

  13. Franklin-Tong VE, Drøbak BK, Allan AC, Watkins PAC, Trewavas AJ (1996) Growth of pollen tubes of Papaver rhoeas is regulated by a slow moving calcium wave propagated by inositol triphosphate. Plant Cell 8:1305–1321

    Article  PubMed  Google Scholar 

  14. Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol 152:1019–1032

    Article  PubMed  Google Scholar 

  15. Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563

    Article  Google Scholar 

  16. Homann U, Tester M (1997) Ca2+-independent and Ca2+=GTP-binding protein-controlled exocytosis in a plant cell. Proc Natl Acad Sci USA 94:6565–6570

    Article  PubMed  Google Scholar 

  17. Kandasamy MK, Kappler R, Kristen U (1988) Plasmatubules in the pollen tubes of Nicotiana sylvestris. Planta 173:35–41

    Article  Google Scholar 

  18. Kang B-H, Rancour DM, Bednarek SY (2003) The dynamin-like protein ADL1C is essential for plasma membrane maintenance during pollen maturation. Plant J 35:1–15

    Article  PubMed  Google Scholar 

  19. Kooijman EE, Chupin V, de Kruijff B, Burger KNJ (2003) Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 4:162–174

    PubMed  Google Scholar 

  20. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua M-H (1999) Rac homologues and compartmentalized phosphatidilinositol 4,4-biphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330

    Article  PubMed  Google Scholar 

  21. Lancelle SA, Hepler PK (1992) Ultrastructure of freeze-substituted pollen tubes of Lilium longiflorum. Protoplasma (1992) 167:215–230

    Article  Google Scholar 

  22. Lancelle SA, Cresti M, Hepler PK (1997) Growth inhibition and recovery in freeze-substituted Lilium longiflorum pollen tubes: structural effects of caffeine. Protoplasma 196:21–33

    Article  Google Scholar 

  23. Lennon KA, Lord EM (2000) The in vivo pollen tube cell of Arabidopsis thaliana I. Tube cell cytoplasm and wall. Protoplasma 214:45–56

    Google Scholar 

  24. Li H, Lin Y, Heath RM, Zhu MX, Yang Z (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731–1742

    Article  PubMed  Google Scholar 

  25. Lin Y, Wang Y, Zhu J-K, Yang Z (1996) Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 8:293–303

    Article  PubMed  Google Scholar 

  26. Ma L, Xu X, Cui S, Sun D (1999) The presence of a heterotrimeric G protein and Its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. Plant Cell 11:1351–1364

    Article  PubMed  Google Scholar 

  27. Malhó R (1998) The role of inositol(1,4,5)triphosphate in pollen tube growth and orientation. Sex Plant Reprod 11:231–235

    Article  Google Scholar 

  28. Malhó R, Trewavas AJ (1996) Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8:1935–1949

    Article  PubMed  Google Scholar 

  29. Malhó R, Camacho L (2004) Signalling the cytoskeleton in pollen tube germination and growth. In: Hussey PJ (ed) The plant cytoskeleton in cell differentiation and development. Annual plant review series. Blackwell London, UK, pp 240–264

    Google Scholar 

  30. Malhó R, Read ND, Trewavas AJ, Pais MS (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7:1173–1184

    Article  PubMed  Google Scholar 

  31. Malhó R, Camacho L, Moutinho A (2000) Signalling pathways in pollen tube growth and reorientation. Ann Bot 85 (Suppl A):59–68

    Google Scholar 

  32. Malhó R, Liu Q, Monteiro D, Rato C, Camacho L, Dinis A (2005) Signalling pathways in pollen germination and tube growth. Protoplasma (in press)

    Google Scholar 

  33. Messerli M, Robinson KR (1997) Tip localized Ca2+pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum. J Cell Sci 110:1269–1278

    PubMed  Google Scholar 

  34. Monteiro D, Castanho Coelho P, Rodrigues C, Camacho L, Quader H, Malhó R (2005a) Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids. Protoplasma (in press)

    Google Scholar 

  35. Monteiro D, Liu Q, Lisboa S, Scherer GEF, Quader H, Malhó R (2005b) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. J Exp Bot 56:1665–1674

    Google Scholar 

  36. Morré DJ, van der Woude WJ (1974) Origin and growth of cell surface components. In: Hay ED, King TJ, Papaconstantinou J (eds) Macromolecules regulating growth and development. Academic, New York, pp 81–111

    Google Scholar 

  37. Moutinho A, Trewavas AJ, Malhó R (1998) Relocation of a Ca2+-dependent protein kinase activity during pollen tube reorientation. Plant Cell 10:1499–1510

    Article  PubMed  Google Scholar 

  38. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233

    Article  PubMed  Google Scholar 

  39. O'Luanaigh N, Pardo R, Fensome A, Allen-Baume V, Jones D, Holt MR, Cockcroft S (2002) Continual production of phosphatidic acid by phospholipase D is essential for antigen-stimulated membrane ruffling in cultured mast cells. Mol Biol Cell 13:3730–3746

    Article  PubMed  Google Scholar 

  40. Parton RM, Fischer-Parton S, Watahiki MK, Trewavas AJ (2001) Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J Cell Sci 114:2685–2695

    PubMed  Google Scholar 

  41. Parton RM, Fischer-Parton S, Trewavas AJ, Watahiki MK (2003) Pollen tubes exhibit regular periodic membrane trafficking events in the absence of apical extension. J Cell Sci 116:2707–2719

    Article  PubMed  Google Scholar 

  42. Picton JM, Steer MW (1981) Determination of secretory vesicle production rates by dictyossomes in pollen tubes of Tradescantia using Cytochalasin D. J Cell Sci 49:261–272

    PubMed  Google Scholar 

  43. Picton JM, Steer MW (1985) The effects of ruthenium red, lanthanum, fluorescein isothiocyanate and trifluoperazine on vesicle transport, vesicle fusion and tip extension in PT. Planta 163:20–26

    Article  Google Scholar 

  44. Pierson ES, Miller DD, Callaham DA, van Aken J, Hackett G, Hepler PK (1996) Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol 174:160–173

    Article  PubMed  Google Scholar 

  45. Powner DJ, Wakelam MJO (2002) The regulation of phospholipase D by inositol phospholipids and small GTPases. FEBS Lett 531:62–64

    Article  PubMed  Google Scholar 

  46. Rato C, Monteiro D, Hepler PK, Malhó R (2004) Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes. Plant J 38:887–897

    Article  PubMed  Google Scholar 

  47. Richards DA, Bai J, Chapman ER (2005) Two modes of exocytosis at hippocampal synapses revealed by rate of FM1-43 efflux from individual vesicles. J Cell Biol 168:929–939

    Article  PubMed  Google Scholar 

  48. Roy S, Eckard KJ, Lancelle S, Hepler PK, Lord EM (1997) High-pressure freezing improves the ultrastructural preservation of in vivo-grown lily pollen tubes. Protoplasma 200:87–98

    Article  Google Scholar 

  49. Roy SJ, Holdaway-Clarke TL, Hackett GR, Kunkel JG, Lord EM, Hepler PK (1999) Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis. Plant J 19:379–386

    Article  PubMed  Google Scholar 

  50. Rutten TLM, Knuiman B (1993) Brefeldin A effects on tobacco pollen tubes. Eur J Cell Biol 61:247–255

    PubMed  Google Scholar 

  51. Šamaj J, Baluška F, Voigt B, Volkmann D, Menzel D (2005) Endocytosis and acto-myosin cytoskeleton (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  52. Schuurink RC, Chan PV, Jones RL (1996) Modulation of calmodulin mRNA and protein levels in barley aleurone. Plant Physiol 111:371–380

    PubMed  Google Scholar 

  53. Smith RM, Baibakov B, Ikebuchi Y, White BH, Lambert NA, Kaczmarek LK, Vogel SS (2000) Exocytotic insertion of calcium channels constrains compensatory endocytosis to sites of exocytosis. J Cell Biol 148:755–767

    Article  PubMed  Google Scholar 

  54. Staiger CJ (2000) Signalling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51:257–288

    Article  PubMed  Google Scholar 

  55. Steer MW, Steer JL (1989) Pollen tube tip growth. New Phytol 111:323–358

    Google Scholar 

  56. Stevenson JM, Perera IY, Heilmann I, Persson S, Boss WF (2000) Inositol signalling and plant growth. Trends Plant Sci 5:252–258

    Article  PubMed  Google Scholar 

  57. Sweeney DA, Siddhanta A, Shields D (2002) Fragmentation and re-assembly of the Golgi apparatus in vitro–-a requirement for phosphatidic acid and phosphatidylinositol 4,5-bisphosphate synthesis. J Biol Chem 77:3030–3039

    Article  Google Scholar 

  58. Taylor LP, Hepler PK (1997) Pollen germination and tube growth. Annu Rev Plant Physiol Plant Mol Biol 48:461–491

    Article  PubMed  Google Scholar 

  59. Trotter PJ, Orchard MA, Walker JH (1995) Ca2+concentration during binding determines the manner in which annexin V binds to membranes. Biochem J 308:591–598

    PubMed  Google Scholar 

  60. Van der Hoeven PCJ, Siderius M, Korthout HAAJ, Drabkin AV, De Boer AH (1996) A calcium and free fatty acid-modulated protein kinase as putative effector of the fusicoccin 14-3-3 receptor. Plant Physiol 111:857–865

    Article  PubMed  Google Scholar 

  61. Vidali L, McKenna ST, Hepler PK (2001) Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12:2534–2545

    PubMed  Google Scholar 

  62. Vidali L, Yokota E, Cheung AY, Shimmen T, Hepler PK (1999) The 135 kDa actin-bundling protein from Lilium longiflorum pollen is the plant homologue of villin. Protoplasma 209:283–291

    Article  Google Scholar 

  63. Yokota E, Muto S, Shimmen T (1999) Inhibitory regulation of higher-plant myosin by Ca2+ ions. Plant Physiol 119:231–239

    Article  PubMed  Google Scholar 

  64. Yokota E, Muto S, Shimmen T (2000) Calcium-calmodulin suppresses the filamentous actin-binding activity of a 135-kilodalton actin-bundling protein isolated from lily pollen tubes. Plant Physiol 123:645–654

    Article  PubMed  Google Scholar 

  65. Yokota E, Shimmen T (1999) The 135-kDa actin-bundling protein from lily pollen tubes arranges F-actin into bundles with uniform polarity. Planta 209:264–266

    Article  PubMed  Google Scholar 

  66. Yokota E, Takahara K, Shimmen T (1998) Actin-bundling protein isolated from pollen tubes of lily: biochemical and immunocytochemical characterization. Plant Physiol 116:1421–1429

    Article  PubMed  Google Scholar 

  67. Zenisek D, Steyer JA, Almers W (2000) Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406:849–854

    Article  PubMed  Google Scholar 

  68. Zheng Z-L, Yang Z (2000) The Rop GTPase switch turns on polar growth in pollen. Trends Plant Sci 5:298–303

    Article  PubMed  Google Scholar 

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Acknowledgments

The work was supported by a UE TMR grant (TIPNET) and Fundação Ciência e Tecnologia, Lisboa, Portugal (grants nos. BCI/37555/2001; BCI/44148/2002; FEDER).

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Authors and Affiliations

  1. Universidade de Lisboa, Faculdade de Ciências de Lisboa, ICAT, 1749-016, Lisbon, Portugal

    Rui Malhó & Pedro Castanho Coelho

  2. Department of Plant Cell Research, Institute for Wetland and Water Research, Faculty of Science, Radboud University Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands

    Elizabeth Pierson & Jan Derksen

Authors
  1. Rui Malhó
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  2. Pedro Castanho Coelho
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  3. Elizabeth Pierson
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  4. Jan Derksen
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Correspondence to Rui Malhó .

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Jozef Šamaj František Baluška Diedrik Menzel

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Malhó, R., Coelho, P.C., Pierson, E., Derksen, J. Endocytosis and Membrane Recycling in Pollen Tubes. In: Šamaj, J., Baluška, F., Menzel, D. (eds) Plant Endocytosis. Plant Cell Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_017

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