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PLANT CELL 14 (9): 2233-2249

Copyright © 2002 by the American Society of Plant Physiologists.

Oscillatory Chloride Efflux at the Pollen Tube Apex Has a Role in Growth and Cell Volume Regulation and Is Targeted by Inositol 3,4,5,6-Tetrakisphosphate

Laura Zonia1,a, Sofia Cordeirob,c, Jaroslav Tupya, and José A. Feijób,c

a Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Na Pernikarce 15, 160 00 Prague 6, Czech Republic
b Instituto Gulbenkian Ciência, R. Quinta Grande 6, PT-2780-156 Oeiras, Portugal
c Centro de Biotecnologia Vegetal, Department Biologia Vegetal, Faculdad Ciênicas da Universitie de Lisboa, Campo Grande Ed. C2, 1749-016 Lisboa, Portugal

1 To whom correspondence should be addressed. E-mail zonia{at}; fax 420-2-33339412

Abstract: Oscillatory growth of pollen tubes has been correlated with oscillatory influxes of the cations Ca2+, H+, and K+. Using an ion-specific vibrating probe, a new circuit was identified that involves oscillatory efflux of the anion Cl- at the apex and steady influx along the tube starting at 12 µm distal to the tip. This spatial coupling of influx and efflux sites predicts that a vectorial flux of Cl- ion traverses the apical region. The Cl- channel blockers 4,4'-diisothiocyanatostilbene-2,2'-disulfonic acid (DIDS) and 5-nitro-2-(3-phenylpropylamino)benzoic acid completely inhibited tobacco pollen tube growth at 80 and 20 µM, respectively. Cl- channel blockers also induced increases in apical cell volume. The apical 50 µm of untreated pollen tubes had a mean cell volume of 3905 ± 75 µm3. DIDS at 80 µM caused a rapid and lethal cell volume increase to 6206 ± 171 µm3, which is at the point of cell bursting at the apex. DIDS was further demonstrated to disrupt Cl- efflux from the apex, indicating that Cl- flux correlates with pollen tube growth and cell volume status. The signal encoded by inositol 3,4,5,6-tetrakisphosphate [Ins(3,4,5,6)P4] antagonized pollen tube growth, induced cell volume increases, and disrupted Cl- efflux. Ins(3,4,5,6)P4 decreased the mean growth rate by 85%, increased the cell volume to 5997 ± 148 µm3, and disrupted normal Cl- efflux oscillations. These effects were specific for Ins(3,4,5,6)P4 and were not mimicked by either Ins(1,3,4,5)P4 or Ins(1,3,4,5,6)P5. Growth correlation analysis demonstrated that cycles of Cl- efflux were coupled to and temporally in phase with cycles of growth. A role for Cl- flux in the dynamic cellular events during growth is assessed. Differential interference contrast microscopy and kymographic analysis of individual growth cycles revealed that vesicles can advance transiently to within 2 to 4 µm of the apex during the phase of maximally increasing Cl- efflux, which temporally overlaps the phase of cell elongation during the growth cycle. In summary, these investigations indicate that Cl- ion dynamics are an important component in the network of events that regulate pollen tube homeostasis and growth.

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B. Tavares, P. Domingos, P. N. Dias, J. A. Feijo, and A. Bicho (2011)
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Spatial and temporal integration of signalling networks regulating pollen tube growth.
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J. Sun, S. Dai, R. Wang, S. Chen, N. Li, X. Zhou, C. Lu, X. Shen, X. Zheng, Z. Hu, et al. (2009)
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   Abstract »    Full Text »    PDF »
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L. L. Ge, H. Q. Tian, and S. D. Russell (2007)
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   Abstract »    Full Text »    PDF »
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P. Campanoni and M. R. Blatt (2007)
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L. Cardenas, S. T. McKenna, J. G. Kunkel, and P. K. Hepler (2006)
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P. E. Dowd, S. Coursol, A. L. Skirpan, T.-h. Kao, and S. Gilroy (2006)
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S. Shabala, L. Shabala, D. Gradmann, Z. Chen, I. Newman, and S. Mancuso (2006)
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   Abstract »    Full Text »    PDF »
Oscillatory ROP GTPase Activation Leads the Oscillatory Polarized Growth of Pollen Tubes.
J.-U. Hwang, Y. Gu, Y.-J. Lee, and Z. Yang (2005)
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R. M. Parton, S. Fischer-Parton, A. J. Trewavas, and M. K. Watahiki (2003)
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Pulsating Ion Fluxes and Growth at the Pollen Tube Tip.
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