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One Thousand and One Oscillators at the Pollen Tube Tip: The Quest for a Central Pacemaker Revisited

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Pollen Tip Growth

Abstract

Pollen tube growth and oscillations constitute a prime system to study polarized cell growth, warranting the expansion of mathematical models in recent years. Although it is unlikely to have a myriad of distinct independent oscillators at the pollen tube tip, the tendency to describe as many new oscillators as there are objects of study is likely to continue. The same process has happened for over 60 years of studies in circadian rhythms and, similarly, in other biological phenomena displaying oscillatory behavior. Here, we take the opportunity to revise pollen tube oscillator models with cautionary tales learned in other systems. Currently the nature of the core negative feedback loop generating the oscillations, as well as the role and regulation of Ca2+ and growth, seems elusive. The vast majority of mathematical models assume that intracellular Ca2+ is primarily controlled by stretch-activated channels and, thus, relies on membrane tension and growth. Counterpoints to these canonical assumptions will be given as to evidence the gaps in achieving a comprehensive view of pollen tube oscillations. Finally, inspiration stemming from systems involving intracellular polarity and chemotaxis motivates a proposal for the existence of two putatively coupled and yet distinct oscillatory systems involved in pollen tube growth: a signaling-based oscillator at the tip and a motion-based oscillator at the shank, which could be coupled by intracellular signals as Ca2+ waves. This proposition may account for the oscillations observed in nongrowing tubes, as both oscillators could be uncoupled in certain regimes, resolving the conundrum entailed by current model.

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References

  • Abraham U, Granada AE, Westermark PO, Heine M, Kramer A, Herzel H (2010) Coupling governs entrainment range of circadian clocks. Mol Syst Biol 6:438

    Article  PubMed  PubMed Central  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. Nat Rev Genet 6:544–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21

    Article  CAS  PubMed  Google Scholar 

  • Bjørnstad ON, Grenfell BT (2001) Noisy clockwork: time series analysis of population fluctuations in animals. Science 293(5530):638–643

    Google Scholar 

  • Blasius B, Huppert A, Stone L (1999) Complex dynamics and phase synchronization in spatially extended ecological systems. Nature 399:354–359

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bodenstein C, Knoke B, Marhl M, Perc M, Schuster S (2010) Using Jensen’s inequality to explain the role of regular calcium oscillations in protein activation. Phys Biol 7:36009

    Article  CAS  Google Scholar 

  • Buzsáki G (2006) Rhythms of the brain. Oxford University Press, Oxford

    Book  Google Scholar 

  • Ciliberto A, Novak B, Tyson JJ (2005) Steady states and oscillations in the p53/Mdm2 network. Cell Cycle 4:488–493

    Article  CAS  PubMed  Google Scholar 

  • Damineli DSC, Portes MT, Feijó JA (2017) Oscillatory signatures underlie growth regimes in Arabidopsis pollen tubes: computational methods to estimate tip location, periodicity, and synchronization in growing cells. J Exp Bot erx032

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–3

    Google Scholar 

  • Edelstein-Keshet L, Holmes WR, Zajac M, Dutot M (2013) From simple to detailed models for cell polarization. Philos Trans R Soc B Biol Sci 368:20130003–20130003

    Article  Google Scholar 

  • Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O’Neill JS, Reddy AB (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 489:590

    Article  CAS  Google Scholar 

  • Endersby J (2009) Lumpers and splitters: Darwin, Hooker, and the search for order. Science 326:1496–1499

    Article  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, 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

    Article  PubMed  Google Scholar 

  • Forger DB, Kronauer RE (2002) Reconciling mathematical models of biological clocks by averaging on approximate manifolds. SIAM J Appl Math 62:1281–1296

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garmendia-Torres C, Goldbeter A, Jacquet M (2007) Nucleocytoplasmic oscillations of the yeast transcription factor Msn2: evidence for periodic PKA activation. Curr Biol 17:1044–1049

    Article  CAS  PubMed  Google Scholar 

  • Geitmann A, Cresti M (1998) Ca2+ channels control the rapid expansions in pulsating growth of Petunia hybrida pollen tubes. J Plant Physiol 152:439–447

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gibb S, Maroto M, Dale JK (2010) The segmentation clock mechanism moves up a notch. Trends Cell Biol 20:593–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldbeter A (1975) Mechanism for oscillatory synthesis of cyclic AMP in Dictyostelium discoideum. Nature 253:540–542

    Article  CAS  PubMed  Google Scholar 

  • Goldbeter A (1995) A model for circadian oscillations in the Drosophila period protein (PER). Proc Biol Sci 261:319–324

    Article  CAS  PubMed  Google Scholar 

  • Goldbeter A, Lefever R (1972) Dissipative structures for an allosteric model. Application to glycolytic oscillations. Biophys J 12:1302–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Granada AE, Herzel H (2009) How to achieve fast entrainment? The timescale to synchronization. PLoS One 4:e7057

    Article  PubMed  PubMed Central  Google Scholar 

  • Granada AE, Cambras T, Diez-Noguera A, Herzel H (2011) Circadian desynchronization. Interface Focus 1:153–166

    Article  PubMed  Google Scholar 

  • Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16:598–610

    Article  CAS  PubMed  Google Scholar 

  • Gu Y, Vernoud V, Fu Y, Yang Z (2003) ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot 54:93–101

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hepler PK, Rounds CM, Winship LJ (2013) Control of cell wall extensibility during pollen tube growth. Mol Plant 6:998–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoeller O, Toettcher JE, Cai H, Sun Y, Huang C-H, Freyre M, Zhao M, Devreotes PN, Weiner OD (2016) Gβ regulates coupling between actin oscillators for cell polarity and directional migration. PLOS Biol 14:e1002381

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffman DA, Sprengel R, Sakmann B (2002) Molecular dissection of hippocampal theta-burst pairing potentiation. Proc Natl Acad Sci USA 99:7740–7745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Hotta CT, Gardner MJ, Hubbard KE, Baek SJ, Dalchau N, Suhita D, Dodd AN, Webb AAR (2007) Modulation of environmental responses of plants by circadian clocks. Plant Cell Environ 30:333–349

    Article  CAS  PubMed  Google Scholar 

  • Huang C-H, Tang M, Shi C, Iglesias PA, Devreotes PN (2013) An excitable signal integrator couples to an idling cytoskeletal oscillator to drive cell migration. Nat Cell Biol 15:1307–1316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang J-U (2005) Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol Biol Cell 16:5385–5399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang J-U, 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. Curr Biol 18:1907–1916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Kroeger J, Geitmann A (2011) Modeling pollen tube growth: feeling the pressure to deliver testifiable predictions. Plant Signal Behav 6:1828–1830

    Google Scholar 

  • Kroeger JH, Geitmann A (2012) Pollen tube growth: getting a grip on cell biology through modeling. Mech Res Commun 42:32–39

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  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:e18549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lema MA, Golombek DA, Echave J (2000) Delay model of the circadian pacemaker. J Theor Biol 204:565–573

    Article  CAS  PubMed  Google Scholar 

  • Lewis J (2003) Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 13:1398–1408

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  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

    PubMed  PubMed Central  Google Scholar 

  • Liu J, Grieson CS, Webb AA, Hussey PJ (2010) Modelling dynamic plant cells. Curr Opin Plant Biol 13:744–749

    Article  CAS  PubMed  Google Scholar 

  • McClung CR (2000) Minireview: Circadian rhythms in plants: a millennial view. Physiol Plant 109:359–371

    Article  CAS  Google Scholar 

  • McClung CR (2001) Circadian rhythms in plants. Annu Rev Plant Physiol Plant Mol Biol 52:139–162

    Article  CAS  PubMed  Google Scholar 

  • McClure AW, Lew DJ (2014) Cell polarity: netrin calms an excitable system. Curr Biol 24:R1050–R1052

    Article  CAS  PubMed  Google Scholar 

  • Meinhardt H (1999) Orientation of chemotactic cells and growth cones: models and mechanisms. J Cell Sci 112:2867–2874

    CAS  PubMed  Google Scholar 

  • Meyer T, Stryer L (1988) Molecular model for receptor-stimulated calcium spiking. Proc Natl Acad Sci USA 85:5051–5055

    Article  CAS  PubMed  PubMed Central  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

    Article  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 an experimental paradigm. Int J Dev Biol 53:1609–1622

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Monk NAM (2003) Oscillatory expression of Hes1, p53, and NF-kappaB driven by transcriptional time delays. Curr Biol 13:1409–1413

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329:1306–1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • van Ooijen G, Millar AJ (2012) Non-transcriptional oscillators in circadian timekeeping. Trends Biochem Sci 37:484–492

    Article  PubMed  Google Scholar 

  • Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95:8660–8664

    Google Scholar 

  • Parekh AB (2011) Decoding cytosolic Ca2+ oscillations. Trends Biochem Sci 36:78–87

    Article  CAS  PubMed  Google Scholar 

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

    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

    Article  CAS  PubMed  Google Scholar 

  • Pierson ES, Li YQ, Zhang HQ, Willemse MTM, Linskens HF, Cresti M (1995) Pulsatory growth of pollen tubes: investigation of a possible relationship with the periodic distribution of cell wall components. Acta Bot Neerl 44:121–128

    Article  Google Scholar 

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

    Google Scholar 

  • Pikovsky A, Rosenblum M, Kurths J (2003) Synchronization: a universal concept in nonlinear sciences. Cambridge University Press, Cambridge

    Google Scholar 

  • Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8:1–13

    Article  Google Scholar 

  • Pomerening JR, Kim SY, Ferrell JE (2005) Systems-level dissection of the cell-cycle oscillator: bypassing positive feedback produces damped oscillations. Cell 122:565–578

    Article  CAS  PubMed  Google Scholar 

  • Portes MT, Damineli DSC, Moreno N, Colaço R, Costa S, Feijó JA (2015) The pollen tube oscillator: integrating biophysics and biochemistry into cellular growth and morphogenesis. In: Mancuso S, Shabala S (eds) Rhythms in plants: dynamic responses in a dynamic environment. Springer, Cham, pp 121–156

    Chapter  Google Scholar 

  • Renvoize S (1991) Thamnocalamus spathaceus and its hundred year flowering cycle. Curtis’s Bot Mag 8:185–194

    Article  Google Scholar 

  • Roenneberg T, Merrow M (2001) Circadian systems: different levels of complexity. Philos Trans R Soc B Biol Sci 356:1687–1696

    Article  CAS  Google Scholar 

  • Roenneberg T, Merrow M (2005) Circadian clocks - the fall and rise of physiology. Mol Cell 6:965–971

    CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero E, Augulis R, Novoderezhkin VI, Ferretti M, Thieme J, Zigmantas D, van Grondelle R (2014) Quantum coherence in photosynthesis for efficient solar-energy conversion. Nat Phys 10:676–682

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuster S, Marhl M, Höfer T (2002) Modelling of simple and complex calcium oscillations. Eur J Biochem 269:1333–1355

    Article  CAS  PubMed  Google Scholar 

  • Stricker J, Cookson S, Bennett MR, Mather WH, Tsimring LS, Hasty J (2008) A fast, robust and tunable synthetic gene oscillator. Nature 456:516–519

    Article  CAS  PubMed  Google Scholar 

  • Strogatz SH (1994) Nonlinear dynamics and chaos: with applications to physics, biology, chemistry, and engineering. Perseus Books, Reading

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welsh DK, Takahashi JS, Kay S (2010) Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol 72:551–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winfree AT (1975) Unclocklike behaviour of biological clocks. Nature 253:315–319

    Article  CAS  PubMed  Google Scholar 

  • Winfree AT (2001) The geometry of biological time. Springer, New York

    Book  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu M, Wu X, De Camilli P (2013) Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations. Proc Natl Acad Sci USA 110:1339–1344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong Y, Huang C-H, Iglesias P, Devreotes PN (2010) Cells navigate with a local-excitation, global-inhibition-biased excitable network. Proc Natl Acad Sci USA 107:17079–17086

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Science Foundation (MCB 1616437/2016) and the University of Maryland.

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Authors and Affiliations

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

    Daniel S. C. Damineli, Maria Teresa Portes & José A. Feijó

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  1. Daniel S. C. Damineli
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  2. Maria Teresa Portes
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  3. José A. Feijó
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Correspondence to Daniel S. C. Damineli .

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  1. Department of Molecular Biology, University of Salzburg, Salzburg, Austria

    Gerhard Obermeyer

  2. Cell Biology Molecular Genetics, University of Maryland, College Park, Maryland, USA

    José Feijó

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Damineli, D.S.C., Portes, M.T., Feijó, J.A. (2017). One Thousand and One Oscillators at the Pollen Tube Tip: The Quest for a Central Pacemaker Revisited. In: Obermeyer, G., Feijó, J. (eds) Pollen Tip Growth. Springer, Cham. https://doi.org/10.1007/978-3-319-56645-0_15

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