Skip to main content
SpringerLink
Log in

The Pollen Tube Oscillator: Integrating Biophysics and Biochemistry into Cellular Growth and Morphogenesis

  • Chapter
  • First Online:
Rhythms in Plants

Abstract

Individual cells generate ultradian rhythms in different systems and levels of organisation. A cell biology approach is necessary to better understand the intrinsic nature of these biological oscillators and their evolutionary significance. In this respect, pollen tubes provide a useful working model because, unlike other cells, their growth can be conveniently followed in vitro and it is known to involve structural, biochemical as well as biophysical oscillations. As commonly seen in complex systems, these oscillations involve almost all cellular components but, in this case, their causal relations have not yet been fully identified. Most studies consider growth as a reference to establish the relation with other oscillating variables, interpreted to be a cause if its peak occurs before and as a consequence if it occurs after that of the variable in question. Today, it is known that this group of oscillating variables include at least ion fluxes and internal free concentrations (calcium, chloride, protons and potassium ), the cytoskeleton, membrane trafficking and cell wall synthesis. Despite the progress made in this domain, however, a central core-controlling mechanism is still missing, and even less is known about how all components interact to produce the macroscopic outcome, i.e. structurally and temporally organised apical growth. In other words, we can see the arms of the clock and many underlying moving parts but still miss which work as pendulum, escapement and anchor. Here, we review the recent advances in this field and critically address some of the pitfalls and inconsistencies in the data and models presently available. Some conceptual outlines and future directions of research are also discussed.

Maria Teresa Portes, Daniel Santa Cruz Damineli, Nuno Moreno, Renato Colaço contributed equally to the manuscript.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Augustine GJ (2001) How does calcium trigger neurotransmitter release? Curr Opin Neurobiol 11:320–326

    CAS  PubMed  Google Scholar 

  • Barnabas B, Fridvalszky L (1984) Adhesion and germination of differently treated maize pollen grains on the stigma. Acta Bot Hungarica 30:329–332

    Google Scholar 

  • Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11:643–660

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beaulieu V, Da Silva N, Pastor-Soler N, Brown CR, Smith PJ, Brown D, Breton S (2005) Modulation of the actin cytoskeleton via gelsolin regulates vacuolar H+-ATPase recycling. J Biol Chem 280:8452–8463

    CAS  PubMed  Google Scholar 

  • Becker JD, Boavida LC, Carneiro J, Haury M, Feijó JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beg AA, Ernstrom GG, Nix P, Davis MW, Jorgensen EM (2008) Protons act as a transmitter for muscle contraction in C. elegans. Cell 132:149–160

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nature Rev 6:544–556

    CAS  Google Scholar 

  • Benkert R, Obermeyer G, Bentrup FW (1997) The turgor pressure of growing lily pollen tubes. Protoplasma 198:1–8

    Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev Mol Cell Biol 4:517–529

    CAS  Google Scholar 

  • Blowers DP, Trewavas AJ (1989) Second messengers: their existence and relationship to proteinkinases. In: Boss W, Moore DJ (eds) Second messengers in plant growth and development. Alan R, Liss, New York, pp 1–28

    Google Scholar 

  • Boavida L, Becker JD, Feijó JA (2005a) The making of gametes in higher plants. Int J Dev Biol 49:595–614

    CAS  PubMed  Google Scholar 

  • Boavida L, Becker JD, Vieira AM, Feijó JA (2005b) Gametophyte interaction and sexual reproduction: how plants make a zygote. Int J Dev Biol 49:615–632

    PubMed  Google Scholar 

  • Bosch M, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cai G, Casino C, Romagnoli S, Cresti M (2005) Pollen cytoskeleton during germination and tube growth. Curr Sci 89:1853–1860

    Google Scholar 

  • Cai G, Faleri C, Del Casino C, Emons AMC, Crest M (2011) Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiol 155:1169–1190

    Google Scholar 

  • Cárdenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol 146:1611–1621

    PubMed Central  PubMed  Google Scholar 

  • Cárdenas L, Lovy-Wheeler A, Wilsen KL, Hepler PK (2005) Actin polymerization promotes the reversal of streaming in the apex of pollen tubes. Cell Motility Cytoskel 61:112–127

    CAS  PubMed  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary-cell walls in flowering plants—consistency of molecular-structure with the physical-properties of the walls during growth. Plant J 3:1–30

    CAS  PubMed  Google Scholar 

  • Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N, Michard E, Feijó JA (2008) Exclusion of a proton ATPase from the apical membrane is associated with cell polarity and tip growth in Nicotiana tabacum pollen tubes. Plant Cell 20:614–634

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chebli Y, Kaneda M, Zerzour R, Geitmann A (2012) The cell wall of the Arabidopsis pollen tube- spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160:1940–1955

    Google Scholar 

  • Chebli Y, Kroeger J, Geitmann A (2013) Transport logistics in pollen tubes. Mol Plant 6:1037–1052

    CAS  PubMed  Google Scholar 

  • Chen CY, Cheung AY, Wu HM (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase regulated pollen tube growth. Plant Cell 15:237–249

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen XH, Bezprozvanny I, Tsien RW (1996a) Molecular basis of proton block of L-type Ca2+ channels. J Gen Physiol 108:363–374

    CAS  PubMed  Google Scholar 

  • Chen Y, Simasko SM, Niggel J, Sigurdson WJ, Sachs F (1996b) Ca2+ uptake in GH3 cells during hypotonic swelling: the sensory role of stretch-activated ion channels. Am J Physiol 270:C1790–C1798

    CAS  PubMed  Google Scholar 

  • Cheung AY, Chen CY, Glaven RH, de Graaf BH, Vidali L, Hepler PK, Wu HM (2002) Rab2GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth. Plant Cell 14:945–962

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheung AY, Wu HM (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Ann Rev Plant Biol 59:547–572

    CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nature Rev Mol Cell Biol 6:850–861

    CAS  Google Scholar 

  • Cosson P, de Curtis I, Pouyssegur J, Griffiths G, Davoust J (1989) Low cytoplasmic pH inhibits endocytosis and transport from the trans-Golgi network to the cell surface. J Cell Biol 108:377–387

    CAS  PubMed  Google Scholar 

  • Davoust J, Gruenberg J, Howell KE (1987) Two threshold values of low pH block endocytosis at different stages. EMBO J 6:3601–3609

    CAS  PubMed Central  PubMed  Google Scholar 

  • de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17:2564–2579

    PubMed Central  PubMed  Google Scholar 

  • Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46:268–278

    CAS  PubMed  Google Scholar 

  • Denninger P, Bleckmann A, Lausser A, Vogler F, Ott T, Ehrhardt DW, Grossmann G (2014) Male-female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Commun 5:4645

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dong H, Pei W, Haiyun R (2012) Actin fringe is correlated with tip growth velocity of pollen tubes. Mol Plant 5:1160–1162

    CAS  PubMed  Google Scholar 

  • Dowd PE, Coursol S, Skirpan AL, Kao TH, Gilroy S (2006) Petunia phospholipase C is involved in pollen tube growth. Plant Cell 18:1438–1453

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dumais J, Shaw SL, Steele CR, Long SR, Ray PM (2006) An anisotropic-viscoplastic model of plant cell morphogenesis by tip growth. Int J Dev Biol 50:209–222

    PubMed  Google Scholar 

  • Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dyson F (2004) A meeting with Enrico Fermi. Nature 427:297

    CAS  PubMed  Google Scholar 

  • Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4:415–420

    CAS  PubMed  Google Scholar 

  • Feijó JA (1999) The pollen tube oscillator: towards the molecular mechanism of tip growth? In: Cresti M, Cai G, Moscatelli A (eds) Fertilization in higher plants: molecular and cytological aspects. Springer, Berlin, pp 317–336

    Google Scholar 

  • Feijó JA, Costa S, Prado AM, Becker JD, Certal AC (2004) Signaling by tips. Curr Opin Plant Biol 7:589–598

    PubMed  Google Scholar 

  • Feijó JA, Malho R, Obermeyer G (1995) Ion dynamics and its possible role during in-vitro pollen germination and tube growth. Protoplasma 187:155–167

    Google Scholar 

  • Feijó JA, Moreno N (2004) Imaging plant cells by two-photon excitation. Protoplasma 223:1–32

    PubMed  Google Scholar 

  • Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK (1999) Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 144:483–496

    PubMed Central  PubMed  Google Scholar 

  • Feijó JA, Sainhas J, Holdaway-Clarke T, Cordeiro MS, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. BioEssays 23:86–94

    PubMed  Google Scholar 

  • Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206:452–460

    CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    CAS  PubMed  Google Scholar 

  • Frietsch S, Wang YF, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104:14531–14536

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fukata M, Nakagawa M, Kaibuchi K (2003) Roles of Rho-family GTPases in cell polarisation and directional migration. Curr Opin Cell Biol 15:590–597

    CAS  PubMed  Google Scholar 

  • Geitmann A, Li Y-Q, Cresti M (1996) The role of the cytoskeleton anddyctiosome activity in the pulsatory growth of Nicotiana tabacum and Petunia hybrida pollen tubes. Bot Acta 109:102–109

    CAS  Google Scholar 

  • Geitmann A, Parre E (2004) The local cytomechanical properties of growing pollen tubes correspond to the axial distribution of structural cellular elements. Sex Plant Reprod 17:9–16

    Google Scholar 

  • Geitmann A, Steer MW (2006) The architecture and properties of the pollen tube cell wall. In: Malhó R (ed) The pollen tube: a cellular and molecular perspective. Plant Cell Monographs. Springer, Berlin, pp 177–200

    Google Scholar 

  • Gilbert D, Lloyd D (2000) The living cell: a complex autodynamic multi-oscillator system? Cell Biol Int 24:569–580

    CAS  PubMed  Google Scholar 

  • Gilbert DA, Ferreira GM (2000) Problems associated with the study of cellular oscillations. Cell Biol Int 24:501–514

    CAS  PubMed  Google Scholar 

  • Goldbeter A (1991) A minimal cascade model for the mitotic oscillator involving cyclin and cdc2 kinase. Proc Natl Acad Sci USA 88:9107–9111

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goldbeter A (1997) Biochemical oscillations and cellular rhythms. Cambridge University Press, Cambridge

    Google Scholar 

  • Goldbeter A, Li Y, Dupont G (1990) Oscillatory dynamics in intercellular communication. Biomed Biochim Acta 49:935–940

    CAS  PubMed  Google Scholar 

  • Gu Y, Fu Y, Dowd P, Li SD, Vernoud V, Gilroy S, Yang ZB (2005) A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 169:127–138

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guern J, Felle H, Mathieu Y, Kurkdjian A (1991) Regulation of intracellular pH in plant cells. Int Rev Cytol 127:111

    CAS  Google Scholar 

  • Gutermuth T, Lassig R, Portes M, Maierhofer T, Romeis T, Borst J, Konrad KR (2013) Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 25:4525–4543

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hamamura Y, Nishimaki M, Takeuchi H, Geitmann A, Kurihara D, Higashiyama T (2014) Live Imaging of calcium spikes during double fertilization in Arabidopsis. Nat Commun 5:4722

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hepler PK (1997) Tip growth in pollen tubes: calcium leads the way. Trends Plant Sci 2:79–80

    Google Scholar 

  • Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187

    CAS  PubMed  Google Scholar 

  • Holdaway-Clarke TL, Feijó JA, Hackett GR, Kunkel JG, Hepler PK (1997) Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9:1999–2010

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Holdaway-Clarke TL, Weddle NM, Kim S, Robi A, Parris C, Kunkel JG, Hepler PK (2003) Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. J Exp Bot 54:65–72

    CAS  PubMed  Google Scholar 

  • Wei-Jie Huang, Hai-Kuan L, McCormick S, Wei-Hua T (2014) Tomato pistil factor STIG1 promotes in vivo pollen tube growth by binding to phosphatidylinositol 3-phosphate and the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 26:2505–2523

    Google Scholar 

  • Hwang JU, Gu Y, Lee YJ, Yang ZB (2005) Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol Biol Cell 16:5385–5399

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hwang JU, Vernoud V, Szumlanski A, Nielsen E, Yang Z (2008) A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Cur Biol 18:1907–1916

    CAS  Google Scholar 

  • Idilli AI, Morandini P, Onelli E, Rodighiero S, Caccianiga M, Moscatelli A (2013) Microtubule depolymerization affects endocytosis and exocytosis in the tip and influences endosome movement in tobacco pollen tubes. Mol Plant 6:1109–1130

    CAS  PubMed  Google Scholar 

  • Iwano M, Entani T, Shiba H, Kakita M, Nagai T, Mizuno H, Miyawaki A, Shoji T, Kubo K, Isogai A (2009) Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol 150:1322–1334

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iwano M, Ngo QA, Entani T, Shiba H, Nagai T, Miyawaki A, Isogai A, Grossniklaus U, Takayama S (2012) Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells. Development 139:4202–4209

    CAS  PubMed  Google Scholar 

  • Iwano M, Shiba H, Miwa T, Che FS, Takayama S, Nagai T, Miyawaki A, Isogai A (2004) Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 136:3562–3571

    CAS  PubMed Central  PubMed  Google Scholar 

  • Konrad KR, Wudick MM, Feijó JA (2011) Calcium regulation of tip growth: new genes for old mechanisms. Curr Opin Plant Biol 14:721–730

    CAS  PubMed  Google Scholar 

  • Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kroeger JH, Geitmann A (2013) Pollen tubes with more viscous cell walls oscillate at lower frequencies. Math Model Nat Pheno 8:25–34

    Google Scholar 

  • Kroeger J, Geitmann A (2012) The pollen tube paradigm revisited. Cur Opin Plant Biol 15:618–624

    Google Scholar 

  • Kroeger JH, Geitmann A, Grant M (2008) Model for calcium dependent oscillatory growth in pollen tubes. J Theor Biol 253:363–374

    CAS  PubMed  Google Scholar 

  • Kroeger JH, Zerzour R, Geitmann A (2011) Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth. PLoS One 6(4):e18549

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kovar DR, Drøbak BK, Staiger CJ (2000) Maize profilin isoforms are functionally distinct. Plant Cell 12:583–598

    Google Scholar 

  • Kuhtreiber WM, Jaffe LF (1990) Detection of extracellular calcium gradients with a calciumspecific vibrating electrode. J Cell Biol 110:1565–1573

    CAS  PubMed  Google Scholar 

  • Kunkel JG, Cordeiro S, Xu J, Shipley AM, Feijó JA (2006) The use of non-invasive ion-selective microelectrode techniques for the study of plant development. In: Volkov V (ed) Plant electrophysiology—Theory and methods. Springer, Berlin, pp 109–137

    Google Scholar 

  • Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T (2014) Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106

    CAS  PubMed  Google Scholar 

  • Lefebvre B, Arango M, Oufattole M, Crouzet J, Purnelle B, Boutry M (2005) Identification of a Nicotiana plumbaginifolia plasma membrane H+-ATPase gene expressed in the pollen tube. Plant Mol Biol 58:775–787

    CAS  PubMed  Google Scholar 

  • Li YQ, Chen F, Linskens HF, Cresti M (1994) Distribution of unesterified and esterified pectins in cell-walls of pollen tubes of flowering plants. Sex Plant Reprod 7:145–152

    Google Scholar 

  • Li YQ, Mareck A, Faleri C, Moscatelli A, Liu Q, Cresti M (2002) Detection and localization of pectin methylesterase isoforms in pollen tubes of Nicotiana tabacum L. Planta 214:734–740

    CAS  PubMed  Google Scholar 

  • Li YQ, Zhang HQ, Pierson ES, Huang FY, Linskens HF, Hepler PK, Cresti M (1996) Enforced growth-rate fluctuation causes pectin ring formation in the cell wall of Lilium longiflorum pollen tubes. Planta 200:41–49

    CAS  Google Scholar 

  • Liu J, Hussey P (2011) Towards the creation of a systems tip growth model for a pollen tube. Plant Signal Behav 6:520–522

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu J, Hussey PJ (2014) Dissecting the regulation of pollen tube growth by modeling the interplay of hydrodynamics, cell wall and ion dynamics. Front Plant Sci 5(392)

    Google Scholar 

  • Liu J, Piette BM a G, Deeks MJ, Franklin-Tong VE, Hussey PJ (2010) A compartmental model analysis of integrative and self-regulatory ion dynamics in pollen tube growth. PloS One 5(10), e13157

    Google Scholar 

  • Lovy-Wheeler A, Cárdenas L, Kunkel JG, Hepler PK (2007) Differential organelle movement on the actin cytoskeleton in lily pollen tubes. Cell Motil Cytoskel 64:217–232

    Google Scholar 

  • Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK (2005) Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221:95–104

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Markova O, Mukhtarov M, Real E, Jacob Y, Bregestovski P (2008) Genetically encoded chloride indicator with improved sensitivity. J Neurosci Methods 170:67–76

    CAS  PubMed  Google Scholar 

  • Matoh T, Kobayashi M (1998) Boron and calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls. J Plant Res 111:179–190

    CAS  Google Scholar 

  • McClure AW, Lew DJ (2014) Cell polarity: netrin calms an excitable system. Cur Biol 24:1050–1052

    Google Scholar 

  • McKenna ST, Kunkel JG, Bosch M, Rounds CM, Vidali L, Winship LJ, Hepler PK (2009) Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. Plant Cell 21:3026–3040

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meijer HJ, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265–306

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Messerli MA, Creton R, Jaffe LF, Robinson KR (2000) Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev Biol 222:84–98

    CAS  PubMed  Google Scholar 

  • Messerli MA, Danuser G, Robinson KP (1999) Pulsatile influxes of H+, K+ and Ca2+ tag growth pulses of Lilium longiflorum pollen tubes. J Cell Sci 112:1497–1509

    CAS  PubMed  Google Scholar 

  • Messerli MA, Robinson KR (1998) Cytoplasmic acidification and current influx follow growth pulses of Lilium longiflorum pollen tubes. Plant J 16:87–91

    CAS  Google Scholar 

  • Messerli MA, Robinson KR (2003) Ionic and osmotic disruptions of the lily pollen tube oscillator: testing proposed models. Planta 217:147–157

    CAS  PubMed  Google Scholar 

  • Messerli MA, Smith PJS, Lewis RC, Robinson KR (2004) Chloride fluxes in lily pollen tubes: a critical reevaluation. Plant J 40:799–812

    CAS  PubMed  Google Scholar 

  • Michard E, Dias P, Feijó JA (2008) Tobacco pollen tubes as cellular models for ion dynamics: improved spatial and temporal resolution of extracellular flux and free cytosolic concentration of calcium and protons using pHluorin and YC3.1 CaMeleon. Sex Plant Reprod 21:169–181

    CAS  Google Scholar 

  • Michard E, Alves F, Feijó JA (2009) The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as experimental paradigm. Int J Dev Biol 53:1609–1622

    CAS  PubMed  Google Scholar 

  • Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Feijó JA (2011) Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332:434–437

    CAS  PubMed  Google Scholar 

  • Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192–195

    PubMed  Google Scholar 

  • Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101:7–12

    CAS  Google Scholar 

  • Mogilner A, Allard J, Wollman R (2012) Cell polarity: quantitative modeling as a tool in cell biology. Science 336:175–179

    CAS  PubMed  Google Scholar 

  • Money N (2001) Functions and evolutionary origin of hyphal turgor pressure. In: Geitmann A, Cresti M, Heath B (eds) Cell biology of fungal and tip growth. NATO Science Series I, Life and Behavioural Sciences, vol 328. IOS Press, Amsterdam, pp 95–109

    Google Scholar 

  • Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci USA 101:10554–10559

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nari J, Noat G, Diamantidis G, Woudstra M, Ricard J (1986) Electrostatic effects and the dynamics of enzyme-reactions at the surface of plant-cells. 3. Interplay between limited cell-wall autolysis, pectin methyl esterase-activity and electrostatic effects in soybean cell-walls. Eur J Biochem 155:199–202

    CAS  PubMed  Google Scholar 

  • Ngo Q, Vogler H, Lituiev DS, Nestorova A, Grossniklaus U (2014) A calcium dialog mediated by the FERONIA pathway controls plant sperm delivery. Dev Cell 29:491–500

    CAS  PubMed  Google Scholar 

  • Novák B, Tyson JJ (2008) Design principles of biochemical oscillators. Nature Rev 9:981–991

    Google Scholar 

  • Onelli E, Idilli A, Moscatelli A (2015) Emerging roles for microtubules in angiosperm pollen tube growth highlight new research cues. Front Plant Sci 6(51)

    Google Scholar 

  • Palanivelu R, Preuss D (2000) Pollen tube targeting and axon guidance: parallels in tip growth mechanisms. Trends Cell Biol 10:517–524

    CAS  PubMed  Google Scholar 

  • Palin R, Geitmann A (2012) The role of pectin in plant morphogenesis. Bio Systems 109:397–402

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, Cresti M, Hepler PK (1994) 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 6:1815–1828

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Pietruszka M (2013) Pressure-induced cell wall instability and growth oscillations in pollen tubes. PLoS One 8(11):e75803

    PubMed Central  PubMed  Google Scholar 

  • Pina C, Pinto F, Feijó JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals novel biological implications for cell growth and division control and gene expression regulation. Plant Physiol 138:744–756

    CAS  PubMed Central  PubMed  Google Scholar 

  • Potocký M, Jones MA, Bezvoda R, Smirnoff N, Žárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751

    PubMed  Google Scholar 

  • Potocký M, Pleskot R, Pejchar P, Vitale N, Kost B, Žárský V (2014) Live-cell imaging of phosphatidic acid dynamics in pollen tubes visualized by Spo20p-derived biosensor. New Phytol 203:483–494

    PubMed  Google Scholar 

  • Prado AM, Colaço R, Moreno N, Silva AC, Feijó JA (2008) Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Mol Plant 1:703–714

    CAS  PubMed  Google Scholar 

  • Rojas ER, Hotton S, Dumais J (2011) Chemically mediated mechanical expansion of the pollen tube cell wall. Biophys J 101:1844–1853

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rounds CM, Hepler PK, Fuller SJ, Winship LJ (2010) Oscillatory growth in lily pollen tubes does not require aerobic energy metabolism. Plant Physiol 152:736–746

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rounds CM, Hepler PK, Winship LJ (2014) The apical actin fringe contributes to localized cell wall deposition and polarized growth in the lily pollen tube. Plant Physiol 166:139–151

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Sanders D, Slayman CL (1982) Control of intracellular pH. Predominant role of oxidative metabolism, not proton transport, in the eukaryotic microorganism Neurospora. J Gen Physiol 80:377–402

    CAS  PubMed  Google Scholar 

  • Shabala S, Babourina O, Newman I (2000) Ion-specific mechanisms of osmoregulation in bean mesophyll cells. J Exp Bot 51:1243–1253

    CAS  PubMed  Google Scholar 

  • Shipley AM, Feijó JA (1999) The use of the vibrating probe technique to study steady extracellular currents during pollen germination and tube growth. In: Cresti M, Cai G, Moscatelli A (eds) Fertilization in higher plants: molecular and cytological aspects. Springer, Berlin, pp 235–252

    Google Scholar 

  • Smith RM, Baibakov B, Lambert NA, Vogel SS (2002) Low pH inhibits compensatory endocytosis at a step between depolarization and calcium influx. Traffic 3:397–406

    CAS  PubMed  Google Scholar 

  • Steer MW, Steer JM (1989) Pollen tube tip growth. New Phytol 136:405–410

    Google Scholar 

  • Tavares B, Dias PN, Domingos P, Moura TF, Feijó JA, Bicho A (2011) Calcium-regulated anion channels in the plasma membrane of Lilium longiflorum pollen protoplasts. New Phytol 192:45–60

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tsai TY-C, Choi YS, Ma W, Pomerening JR, Tang C, Ferrell JE (2008) Robust, tunable biological oscillations from interlinked positive and negative feedback loops. Science 321:126–129

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vidali L, van Gisbergen PAC, Guerin C, Franco P, Li M, Burkart GM, Augustine RC, Blanchoin L, Bezanilla M (2009) Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc Natl Acad Sci USA 106:13341–13346

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vogler H, Draeger C, Weber A, Felekis D, Eichenberger C, Routier-Kierzkowska AL, Boisson-Dernier A, Ringli C, Nelson BJ, Smith RS, Grossniklaus U (2013) The pollen tube: a soft shell with a hard core. Plant J 73:617–627

    Google Scholar 

  • Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weisenseel MH, Jaffe LF (1976) The major growth current through the lily pollen tube enters as K+ and leaves as H+. Planta 133:1–7

    CAS  PubMed  Google Scholar 

  • Weisenseel MH, Nuccitelli R, Jaffe LF (1975) Large electrical currents traverse growing pollen tubes. J Cell Biol 66:556–567

    CAS  PubMed  Google Scholar 

  • Wen FS, Zhu YM, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140

    CAS  PubMed Central  PubMed  Google Scholar 

  • White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: a review. Ann Bot 88:967–988

    CAS  Google Scholar 

  • Willats WGT, Orfila C, Limberg G, Buchholt HC, van Alebeek GJWM, Voragen AGJ, Marcus SE, Christensen TMIE, Mikkelsen JD, Murray BS, Knox JP (2001) Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls—Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem 276:19404–19413

    CAS  PubMed  Google Scholar 

  • Winship L, J Obermeyer G, Geitmann A, Hepler PK (2011) Pollen tubes and the physical world. Trends Plant Sci 16:353–355

    Google Scholar 

  • Winship L, J Obermeyer, G Geitmann A, Hepler PK (2010) Under pressure, cell walls set the pace. Trends Plant Sci 15:363–369

    Google Scholar 

  • Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249:169–175

    CAS  Google Scholar 

  • Wu CF, Lew DJ (2013) Beyond symmetry-breaking: competition and negative feedback in GTPase regulation. Trends in Cell Biol 23:476–483

    CAS  Google Scholar 

  • Wudick MM, Feijó JA (2014) At the Intersection: merging Ca2+ and ROS signaling pathways in pollen. Mol Plant 7:1595–1597

    CAS  PubMed  Google Scholar 

  • Yan A, Xu G, Yang Z-B (2009) Calcium participates in feedback regulation of the oscillating ROP1 Rho GTPase in pollen tubes. Proc Natl Acad Sci USA 106:22002–22007

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yonezawa N, Nishida E, Sakai H (1985) pH control of actin polymerization by cofilin. J Biol Chem 260:14410–14412

    CAS  PubMed  Google Scholar 

  • Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nature Rev Mol Cell Biol 2:107–117

    CAS  Google Scholar 

  • Zhao Y, Araki S, Wu J, Teramoto T, Chang YF, Nakano M, Abdelfattah AS, Fujiwara M, Ishihara T, Nagai T, Campbell RE (2011) An expanded palette of genetically encoded Ca2+ indicators. Science 333:1888–1891

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zonia L (2010) Spatial and temporal integration of signaling networks regulating pollen tube growth. J Exp Bot 61:1939–1967

    CAS  PubMed  Google Scholar 

  • Zonia L, Cordeiro S, Feijó JA (2001) Ion dynamics and the control of hydrodynamics in the regulation of pollen tube growth. Sex Plant Reprod 14(1/2):111–116

    CAS  Google Scholar 

  • Zonia L, Cordeiro S, Tupy J, Feijó JA (2002) 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. Plant Cell 14:2233–2249

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zonia L, Munnik T (2007) Life under pressure: hydrostatic pressure in cell growth and function. Trend Plant Sci 12:90–97

    CAS  Google Scholar 

  • Zonia L, Munnik T (2011) Understanding pollen tube growth: the hydrodynamic model versus the cell wall model. Trend Plant Sci 16:347–352

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cell Biology and Molecular Genetics Department, University of Maryland, College Park, Maryland, 20742-5815, USA

    Maria Teresa Portes, Daniel Santa Cruz Damineli & José A. Feijó

  2. Instituto Gulbenkian de Ciência, 2780-156, Oeiras, Portugal

    Maria Teresa Portes, Nuno Moreno, Renato Colaço, Sílvia Costa & José A. Feijó

  3. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge, CB2 3EG, UK

    Renato Colaço

Authors
  1. Maria Teresa Portes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Santa Cruz Damineli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nuno Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Renato Colaço
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sílvia Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. José A. Feijó
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José A. Feijó .

Editor information

Editors and Affiliations

  1. Dipartimento di Scienze delle Produzioni Agroalimentari e dell'Ambiente, LINV–International Lab for Plant Neurobiology, University of Florence, Sesto Fiorentino, Italy

    Stefano Mancuso

  2. School of Land and Food, University of Tasmania, Hobart, Tasmania, Australia

    Sergey Shabala

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Portes, M.T., Damineli, D.S.C., Moreno, N., Colaço, R., Costa, S., Feijó, J.A. (2015). The Pollen Tube Oscillator: Integrating Biophysics and Biochemistry into Cellular Growth and Morphogenesis. In: Mancuso, S., Shabala, S. (eds) Rhythms in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-20517-5_6

Download citation

Publish with us

Policies and ethics

Search

Navigation