Pollen Tubes and Tip Growth: of Biophysics and Tipomics



Pollen is the male gametophyte of higher plants and is responsible for the successful transport of the sperm cells to the ovules. After landing on a stigma, pollen grains will germinate and grow a pollen tube through the stigma and style tissue towards the ovules, where fertilization takes place. In terms of cell biology, the elongation of the pollen tube is characterized by a dramatically polarized growth process, tip growth, which is common to root hairs, fungal hyphae and some developing neurites. Due to their simple morphology and function, growing pollen tubes became the most well-established model system to study tip growth. Both the editors of this book have been enthusiastic paladins of this trend, even since they first met in 1994 during the 13th International Congress on Sexual Plant Reproduction in Vienna. Our intellectual enthusiasm was first materialized in an essay in which a naive and simple yet forward theoretical model was set forth, implying a set of electrochemistry rules to be at the core of a minimal set of mechanism underlying cell polarity establishment and maintenance during pollen tube growth (Feijó et al. ). In short, subcellular biophysical processes, like ion transport, endogenous electrical fields and a tip-focussed Ca2+ gradient, would regulate the shape and growth rate in an essentially self-organizing process. Ever since then, the multitude of nuts and bolts and genes and pathways and their biological consequences have amounted to a vast literature in practically every aspect of the biology of pollen. And yet, some of the essential parts of this naive biophysical view of the pollen tube remained elusive, namely the existence and features of the channels responsible for the unique ion biology of pollen (Michard et al.).


Biophysics Molecular mechanisms Omics techniques Pollen Systems pollen biology Tip growth Tipomics 


  1. Arrivault S, Guenther M, Florian A, Encke B, Feil R, Vosloh D, Lunn JE, Sulpice R, Fernie AR, Stitt M, Schulze WX (2014) Dissecting the subcellular compartmentation of proteins and metabolites in Arabidopsis leaves using non-aqueous fractionation. Mol Cell Proteomics 13:2246–2259CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bibikova TN, Assmann S, Gilroy S (2004) Ca2+ and pH as integrated signals in transport control. In: Blatt MR (ed) Membrane transport in plants, Annual plant reviews, vol 15. Blackwell, Oxford, pp 252–278Google Scholar
  3. Carvalho PC, Lima DB, Leprevost FV, Santos MDM, Fischer JSG, Aquino PF, Moresco JJ, Yates JR III, Barbosa VC (2016) Integrated analysis of shotgun proteomic data with PatternLab for proteomics 4.0. Nat Protoc 11:102–117CrossRefPubMedGoogle Scholar
  4. Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N, Michard E, Carneiro J, Rodriguez-Leon J, Wu H-M, Cheung AY, Feijo J (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 20:614–634CrossRefPubMedPubMedCentralGoogle Scholar
  5. Christoforou A, Mulvey CM, Breckels LM, Geladaki A, Hurrell T, Hayward PC, Naake T, Gatto L, Viner R, Martinez Arias A, Lilley KS (2016) A draft map of the mouse pluripotent stem cell spatial proteome. Nat Commun 7. doi: 10.1038/ncomms9992
  6. Coruzzi GM, Gutiérrez RA (2009) Plant systems biology. In: Annual plant reviews, vol 35. Wiley-Blackwell, OxfordGoogle Scholar
  7. Dunkley TPJ, Hester S, Shadford IP, Runions J, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, Watson RB, Dupree P, Lilley KS (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci USA 103:6518–6523CrossRefPubMedPubMedCentralGoogle Scholar
  8. Feijó JA, Moreno N (2004) Imaging plant cells by two-photon excitation. Protoplasma 223:1–32CrossRefPubMedGoogle Scholar
  9. Feijó JA, Malhó R, Obermeyer G (1995) Ion dynamics and its possible role during in vitro pollen germination and tube growth. Protoplasma 187:155–167CrossRefGoogle Scholar
  10. Feijó JA, Sainhas J, Holdaway-Clarke T, Cordeiro S, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioessays 23:86–94CrossRefPubMedGoogle Scholar
  11. Hamers D, van Voorst VL, Borst JW, Goedhart J (2014) Development of FRET biosensors for mammalian and plant systems. Protoplasma 251:333–347CrossRefPubMedGoogle Scholar
  12. Holdaway-Clarke T, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563CrossRefGoogle Scholar
  13. Humphrey SJ, Azimifar SB, Mann M (2015) High-throughput phosphoproteomics reveals in vivo insulin signaling dynamics. Nat Biotechnol 33:990–995CrossRefPubMedGoogle Scholar
  14. Ingalls BP (2013) Mathematical modeling in systems biology. MIT Press, CambridgeGoogle Scholar
  15. Klipp E, Liebermeister W, Wierling C, Kowald A, Lehrach H, Herwig R (2009) Systems biology. A textbook. Wiley Blackwell, WeinheimGoogle Scholar
  16. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N-H (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330CrossRefPubMedPubMedCentralGoogle Scholar
  17. Krueger S, Giavalisco P, Krall L, Steinhauser M-C, Büssis D, Usadel B, Flügge U-I, Fernie AR, Willmitzer L, Steinhauser D (2011) A topological map of the compartmentalized Arabidopsis thaliana leaf metabolome. PLoS One 6:e17806CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kumar A, Wu Y, Christensen R, Chandris P, Gandler W, McCreedy E, Bokinsky A, Colón-Ramos DA, Bao Z, McAuliffe M, Rondeau G, Shroff H (2014) Dual-view plane illumination microscopy for rapid and spatially isotropic imaging. Nat Protoc 9:2555–2573CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kunkel JG, Cordeiro S, Xu Y, Shipley AM, Feijó JA (2006) Use of non-invasive ion-selective microelectrode techniques for the study of plant development. In: Volkov AG (ed) Plant electrophysiology. Theory and methods. Springer, Berlin, pp 110–137Google Scholar
  20. Liu F, Rijkers DTS, Post H, Heck AJR (2015) Proteome-wide profiling of protein assemblies by cross-linking mass spectrometry. Nat Methods. doi: 10.1038/NMETH.3603 Google Scholar
  21. Maizel A, von Wangenheim D, Federici F, Haseloff J, Stelzer EHK (2011) High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J 68:377–385CrossRefPubMedGoogle Scholar
  22. Michalski A, Damoc E, Hauschild J-P, Lange O, Wieghaus A, Makarov A, Nagaraj N, Cox J, Mann M, Horning S (2011) Mass spectrometry-based proteomics using Q exactive, a high-performance benchtop quadrupole orbitrap mass spectrometer. Mol Cell Proteomics 10. doi: 10.1074/mcp.M111.011015-1
  23. Michalski A, Damoc E, Lange O, Denisov E, Nolting D, Müller M, Viner R, Schwartz J, Remes P, Belford M, Dunyach J-J, Cox J, Horning S, Mann M, Makarov A (2012) Ultra high resolution linear ion trap orbitrap mass spectrometer (Orbitrap Elite) facilitates top down LC MS/MS and versatile peptide fragmentation modes. Mol Cell Proteomics 11. doi: 10.1074/mcp.O111.013698–1
  24. Michard E, Dias P, Feijo 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 21:169–181CrossRefGoogle Scholar
  25. Michard E, Simon AA, Tavares B, Wudick MM, Feijo JA (2017) Signaling with ions: the keystone for apical cell growth and morphogenesis in pollen tubes. Plant Physiol 173:91–111CrossRefPubMedGoogle Scholar
  26. Monteiro D, Liu Q, Lisboa S, Scherer GEF, Quader H, Malhó R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. J Exp Bot 56:1665–1674CrossRefPubMedGoogle Scholar
  27. Ntranos V, Kamath GM, Zhang JM, Pachter L, Tse DN (2016) Fast and accurate single-cell RNA-seq analysis by clustering of transcript-compatibility counts. Genome Biol 17:112. doi: 10.1186/s13059-016-0970-8 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Okumoto S, Jones A, Frommer WB (2012) Quantitative imaging with fluorescent biosensors. Annu Rev Plant Biol 63:663–706CrossRefPubMedGoogle Scholar
  29. Pertl H, Himly M, Gehwolf R, Kriechbaumer R, Strasser D, Michalke W, Richter K, Ferreira F, Obermeyer G (2001) Molecular and physiological characterisation of a 14-3-3 protein from lily pollen grains regulating the activity of the plasma membrane H+ ATPase during pollen grain germination and tube growth. Planta 213:132–141CrossRefPubMedGoogle Scholar
  30. Pertl-Obermeyer H, Wu XN, Schrodt J, Müdsam C, Obermeyer G, Schulze WX (2016) Identification of cargo for adaptor protein complexes AP-3 and AP-4 by sucrose gradient profiling. Mol Cell Proteomics 15. doi: 10.1074/mcp.M116.060129
  31. Potocky M, Elias M, Profotova B, Novotna Z, Valentova O, Zarsky V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217:122–130PubMedGoogle Scholar
  32. Schleifenbaum F, Elgass K, Sackrow M, Caesar K, Berendzen K, Meixner AJ, Harter K (2009) Fluorescence intensity decay shape analysis microscopy (FIDSAM) for quantitative and sensitive live-cell imaging: a novel technique for fluorescence microscopy of endogenously expressed fusion proteins. Mol Plant 3:555–562CrossRefPubMedGoogle Scholar
  33. Steinhorst L, Mähs A, Ischebeck T, Zhang C, TZhang X, Arendt S, Schültke S, Heilmann I, Kudla J (2015) Vacuolar CBL-CIPK12 Ca2+-sensor-kinase complexes are required for polarized pollen tube growth. Curr Biol 25:475–482CrossRefGoogle Scholar
  34. Swanson SJ, Choi W-G, Chanoca A, Gilroy S (2011) In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants. Annu Rev Plant Biol 62:273–297CrossRefPubMedGoogle Scholar
  35. Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods. doi: 10.1038/nmeth.3901 PubMedGoogle Scholar
  36. Wang H, Zhuang X, Wang X, Law AHY, Zhao T, Du S, Loy MMT, Jiang L (2016) A distinct pathway for polar exocytosis in plant cell wall formation. Plant Physiol 172:1003–1018PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Molecular Plant Biophysics and Biochemistry, Department of Molecular BiologyUniversity of SalzburgSalzburgAustria
  2. 2.Department of Cell Biology and Molecular GeneticsUniversity of MarylandCollege ParkUSA

Personalised recommendations