Hostname: page-component-745bb68f8f-l4dxg Total loading time: 0 Render date: 2025-01-27T14:12:01.379Z Has data issue: false hasContentIssue false
  • English
  • Français

Pollen Tubes With More Viscous Cell Walls Oscillate at LowerFrequencies

Published online by Cambridge University Press:  10 July 2013

J. H. Kroeger  and
A. Geitmann
J. H. Kroeger
Affiliation:
Raymor Nanotech, Boisbriand, Québec, Canada
A. Geitmann*
Affiliation:
Département de sciences biologiques, Institut de recherche en biologie végétale, Université de Montréal, Montréal, Québec, Canada
*
⋆ Corresponding author. E-mail: [email protected]
Get access

Abstract

Pollen tubes are tip growing plant cells that display oscillatory growth behavior. It hasbeen demonstrated experimentally that the reduction of the average pollen tube growth ratethrough elevated extracellular calcium or borate concentrations coincides with a greateramplitude of the growth rate oscillation and a lower oscillation frequency. We present asimple numerical model of pollen tube growth that reproduces these results, as well asanalytical calculations that suggest an underlying mechanism. These data show that thepollen tube oscillator is non-isochronous, and is different from harmonic oscillation.

Keywords

pollen tube growthoscillationsboratecalciumharmonic oscillatormodelling
Type
Research Article
Information
Mathematical Modelling of Natural Phenomena , Volume 8 , Issue 4: Plant growth modelling , 2013 , pp. 25 - 34
Copyright
© EDP Sciences, 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bou Daher, F., Geitmann, A.. Actin is involved in pollen tube tropism through redefining the spatial targeting of secretory vesicles. Traffic, 12 (2011), 1537–1551. CrossRefGoogle ScholarPubMed
Chavarría-Krauser, A., Yejie, D.. A model of plasma membrane flow and cytosis regulation in growing pollen tubes. J. of Theor. Biol., 285 (2011), 10–24. CrossRefGoogle ScholarPubMed
Chebli, Y., Geitmann, A.. Mechanical principles governing pollen tube growth. Functional Plant Science and Biotechnology, 1 (2007), 232–245. Google Scholar
Dumais, J., Long, S.R., Shaw, S.L.. The mechanics of surface expansion anisotropy in Medicago truncatula root hairs. Plant Physiology, 136 (2004), 3266–3275. CrossRefGoogle ScholarPubMed
Dumais, J., Shaw, S.L., Steele, C.R., Long, S.R., Ray, P.M.. An anisotropic-viscoplastic model of plant cell morphogenesis by tip growth. International Journal of Developmental Biology, 50 (2006), 209–222. CrossRefGoogle ScholarPubMed
Dutta, R., Robinson, K.R.. Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol., 135 (2004), 1398–1406. CrossRefGoogle ScholarPubMed
Eggen, E., de Keijser, M.N., Mulder, B.M.. Self-regulation in tip-growth: The role of cell wall aging. Journal of Theoretical Biology, 283 (2011), 113–121. CrossRefGoogle Scholar
Fayant, P., Girlanda, O., Chebli, Y., Aubin, C.E., Villemure, I., Geitmann, A.. Finite element model of polar growth in pollen tubes. Plant Cell, 22 (2010), 2579–2593. CrossRefGoogle ScholarPubMed
Fleischer, A., Titel, C., Ehwald, R.. The boron requirement and cell wall properties of growing and stationary suspensioncultured Chenopidium album L. cells. Plant Physiology, 117 (1998), 1401–1410. CrossRefGoogle Scholar
Fleischer, A., O’Neill, M.A., Ehwald, R.. The pore size of nongraminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiology, 121 (1999), 829–838. CrossRefGoogle ScholarPubMed
A. Geitmann, M.W. Steer. The architecture and properties of the pollen tube cell wall. In: R. Malhó (Ed) The Pollen Tube: A Cellular and Molecular. Perspective, Plant Cell Monographs, Springer Verlag, Berlin, 2006.
Hill, A.E., Shachar-Hill, B., Skepper, J.N., Powell, J., Shachar-Hill, Y.. An osmotic model of the growing pollen tube. PLoS One, 7 (2012), e36585. CrossRefGoogle ScholarPubMed
Holdaway-Clarke, T. L., Weddle, N. M., Kim, S., Robi, A., Parris, C., Kunkel, J. G., Hepler, P. K.. Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. Journal of Experimental Botany, 54 (2003), 65–72. CrossRefGoogle ScholarPubMed
Holdaway-Clarke, T. L., Hepler, P.K.. Tansley Review. Control of pollen tube growth: role of ion gradients and fluxes. New Phytologist 159 (2003). 539–563. CrossRefGoogle Scholar
Ishii, T., Matsunaga, T., Hayashi, N.. Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiology, 126 (2001), 1698–1705. CrossRefGoogle ScholarPubMed
Li, H., Lin, Y., Heath, R.M., Zhu, M.X., Yang, Z.. Control of pollen tube growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell, 11 (1999), 1731–1742. Google ScholarPubMed
Lockhart, J.A.. An analysis of irreversible plant cell elongation. Journal of Theoretical Biology, 8 (1965), 264–275. CrossRefGoogle ScholarPubMed
Kroeger, J. H., Zerzour, R., Geitmann, A.. Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth. PLoS One, 6 (2011), e18549. CrossRefGoogle ScholarPubMed
Kroeger, J. H., Bou Daher, F., Grant, M., Geitmann, A.. Microfilament orientation constrains vesicle flow and spatial distribution in growing pollen tubes. Biophysical Journal, 97 (2009), 1822–1831. CrossRefGoogle ScholarPubMed
Kroeger, J.H., Geitmann, A., Grant, M.. Model for calcium dependent oscillatory growth in pollen tubes. Journal of Theoretical Biology, 253 (2008), 363–374. CrossRefGoogle ScholarPubMed
Kroeger, J.H., Geitmann, A.. Pollen tube growth: Getting a grip on cell biology through modeling. Mechanical Research Communications, 42 (2012), 32–39. CrossRefGoogle Scholar
Leoni, M., Liverpool, T. B.. Hydrodynamic synchronisation of non-linear oscillators at low Reynolds number. Phys. Rev. E 85 (2012). 040901. CrossRefGoogle Scholar
Liu, J., Piette, B.M.A.G., Deeks, M.J., Franklin-Tong, V. E., Hussey, P.J.. A compartmental model analysis of integrative and self-regulatory ion dynamics in pollen tube growth. PLoS One, 5 (2010), e13157. CrossRefGoogle ScholarPubMed
Matoh, T., Kobayashi, M.. Boron and calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls. Journal of Plant Research, 111 (1998), 179–190. CrossRefGoogle Scholar
McKenna, S.T., Kunkel, J.G., M.B. Rounds, C.M., Vidali, L., Winship, L.J., Hepler, P.K. Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. Plant Cell, 21 (2009), 3026–3040. CrossRefGoogle Scholar
Ortega, J.K.E.. Governing equations for plant cell growth. Physiologia Plantarum, 79 (1990), 116–121. CrossRefGoogle Scholar
Ridley, B.L., O’Neill, M.A., Mohnen, D.A.. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry, 57 (2001), 929–967. CrossRefGoogle ScholarPubMed
J. Rinzel. Bursting oscillations in an excitable membrane model, in ordinary and partial differential equations. In: Sleeman BD, Jarvis RJ, editors. Lecture Notes in Mathematics. (1985) New York: Springer. pp. 304–316.
Rojas, E., Hotton, S., Dumais, J.. Chemically mediated mechanical expansion of the pollen tube cell wall. Biophysical Journal, 101 (2011), 1844–1853. CrossRefGoogle ScholarPubMed
Roy, S.J., Holdaway-Clarke, T.L., Hackett, G.R., Kunkel, J.G., Lord, E.M., Helpler, P.K.. Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis. The Plant Journal 19 (1999), 379–386. CrossRefGoogle Scholar
Ullah, G., Jung, P., Cornell-Bell, A.. Antiphase calcium oscillations in astrocytes via inositol (1,4,5)-trisphosphate regeneration. Cell Calcium, 39 (2006) 197208. CrossRefGoogle Scholar
Winship, L.J., Obermeyer, G., Geitmann, A., Hepler, PK.. 2010. Under pressure, cell walls set the pace. Trends in Plant Science 15: 363–369. CrossRefGoogle ScholarPubMed
Yan, A., Xu, G., Yang, Z.-B.. Calcium participates in feedback regulation of the oscillating ROP1 Rho GTPase in pollen tubes. P.N.A.S., 106 (2009), 22002–22007. CrossRefGoogle Scholar
Zerzour, R., Kroeger, J.H., Geitmann, A.. Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev. Biol., 334 (2009) 437–446. CrossRefGoogle ScholarPubMed
Zonia, L., Munnik, T.. Uncovering hidden treasures in pollen tube growth mechanics. Trends Plant Sci., 14 (2009), 318-327. CrossRefGoogle ScholarPubMed
Zonia, L., Munnik, T.. Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. Journal of Experimental Botany, 59 (2008), 861–873. CrossRefGoogle ScholarPubMed