Measuring Cytomechanical Forces on Growing Pollen Tubes



Cytomechanical measurements are important to unravel the influence of the biochemical composition of the plant cell wall on growth, morphogenesis, and stability. Agronomical research has a great interest in cell wall mechanics because in an ideal situation, crop plants grow as fast and large as possible without loosing the strength to withstand destabilizing environmental influences. Pollen tubes provide a convenient system to study major aspects of cytomechanics. They grow extremely fast but expansion is restricted to the tip region, providing a cellular model where both biochemical and mechanical properties vary spatio-temporally along the cell. The path of the pollen tube from the stigma to the ovary is full of obstacles, which the pollen tube has to overcome to reach the ovule and achieve fertilization. Once an obstruction is sensed, it can be either circumvented or penetrated, which involves mechanosensing, signal transduction, internal physiological changes, and adaptation of the mechanical properties of the pollen tube. As a result, the pollen tube changes its growth direction or increases the pushing force, both of which are controlled by a fine-tuned interplay between turgor pressure and cell wall extensibility. In this chapter, we provide an overview of state-of-the-art methods to measure those two parameters, as well as an outlook on novel technical developments that will allow the precise evaluation of the mechanical properties of the cell wall along the length of the pollen tube.


AFM Cell wall CFM Cytomechanics MEMS force sensor Pollen tube Turgor 


  1. Agudelo CG, Nezhad AS, Ghanbari M, Naghavi M, Packirisamy M, Geitmann A (2013) TipChip: a modular MEMS-based platform for experimentation and phenotyping of tip-growing cells. Plant J 73:1057–1068CrossRefPubMedGoogle Scholar
  2. Bechinger C, Giebel KF, Schnell M, Leiderer P, Deising HB, Bastmeyer B (1999) Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285:1896–1899CrossRefPubMedGoogle Scholar
  3. Beck WA (1929) Determining the osmotic value at incipient plasmolysis. Trans Am Microsc Soc 48:204–208CrossRefGoogle Scholar
  4. Benkert R, Obermeyer G, Bentrup FW (1997) The turgor pressure of growing lily pollen tubes. Protoplasma 198:1–8CrossRefGoogle Scholar
  5. Berry PM, Sylvester-Bradley R, Berry S (2006) Ideotype design for lodging-resistant wheat. Euphytica 154:165–179CrossRefGoogle Scholar
  6. Beyeler F, Muntwyler S, Nelson B (2009) A six-axis MEMS force-torque sensor with micro-newton and nano-newtonmeter resolution. J Microelectromech Syst 18:433–441CrossRefGoogle Scholar
  7. Bolduc JF, Lewis LJ, Aubin CE, Geitmann A (2006) Finite-element analysis of geometrical factors in micro-indentation of pollen tubes. Biomech Model Mechan 5:227–236CrossRefGoogle Scholar
  8. Bove J, Vaillancourt B, Kroeger J, Hepler PK, Wiseman PW, Geitmann A (2008) Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiol 147:1646–1658CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burri JT, Hu C, Shamsudhin N, Wang X, Vogler H, Grossniklaus U, Nelson BJ (2016) Dual-axis cellular force microscope for mechanical characterization of living plant cells. In: Proceedings of 12th Conference on Automation Science and Engineering (CASE2016), Fort Worth, USAGoogle Scholar
  10. Chae K, Zhang K, Zhang L, Morikis D, Kim ST, Mollet JC, de la Rosa N, Tan K, Lord EM (2007) Two SCA (stigma/style cysteine-rich adhesin) isoforms show structural differences that correlate with their levels of in vitro pollen tube adhesion activity. J Biol Chem 282:33,845–33,858CrossRefGoogle Scholar
  11. 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 160:1940–1955CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cheung AY, Palanivelu R, Tang WH, Xue HW, Yang WC (2013) Pollen and plant reproduction biology: blooming from east to west. Mol Plant 6:995–997CrossRefPubMedGoogle Scholar
  13. Ciampolini F, Cresti M, Sarfatti G, Tiezzi A (1981) Ultrastructure of the stylar canal cells of Citrus limon (Rutaceae). Plant Syst Evol 138:263–274CrossRefGoogle Scholar
  14. Clair B, Thibaut B, Ramonda M, Lévèque G, Arinero R (2003) Imaging the mechanical properties of wood cell wall layers by atomic force modulation microscopy. IAWA J 24:223–230CrossRefGoogle Scholar
  15. Cosgrove DJ (2016) Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot 67:463–476CrossRefPubMedGoogle Scholar
  16. Crook MJ, Ennos AR (1995) The effect of nitrogen and growth regulators on stem and root characteristics associated with lodging in two cultivars of winter wheat. J Exp Bot 46:931–938CrossRefGoogle Scholar
  17. De T, Chettoor AM, Agarwal P, Salapaka MV, Nettikadan S (2010) Immobilization method of yeast cells for intermittent contact mode imaging using the atomic force microscope. Ultramicroscopy 110:254–258CrossRefPubMedGoogle Scholar
  18. Di Carlo D (2012) A mechanical biomarker of cell state in medicine. J Lab Autom 17:32–42CrossRefPubMedGoogle Scholar
  19. Dimarco RD, Nice CC, Fordyce JA (2012) Family matters: effect of host plant variation in chemical and mechanical defenses on a sequestering specialist herbivore. Oecologia 170:687–693CrossRefPubMedGoogle Scholar
  20. Elleman CJ, Franklin-Tong V, Dickinson HG (1992) Pollination in species with dry stigmas: the nature of the early stigmatic response and the pathway taken by pollen tubes. New Phytol 121:413–424CrossRefGoogle Scholar
  21. Engelhardt H, Sackmann E (1988) On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields. Biophys J 54:495–508CrossRefPubMedPubMedCentralGoogle Scholar
  22. Favre M, Polesel-Maris J, Overstolz T, Niedermann P, Dasen S, Gruener G, Ischer R, Vettiger P, Liley M, Heinzelmann H, Meister A (2011) Parallel AFM imaging and force spectroscopy using two-dimensional probe arrays for applications in cell biology. J Mol Recognit 24:446–452CrossRefPubMedGoogle Scholar
  23. Felekis D, Muntwyler S, Vogler H, Beyeler F, Grossniklaus U, Nelson B (2011) Quantifying growth mechanics of living growing plant cells in situ using microrobotics. Micro Nano Lett 6:311–316CrossRefGoogle Scholar
  24. Felekis D, Vogler H, Grossniklaus U, Nelson BJ (2015a) Microrobotic tools for plant biology. In: Micro- and nanomanipulation tools. Wiley-VCH Verlag GmbH and Co. KGaA, Weinheim, pp 283–306Google Scholar
  25. Felekis D, Vogler H, Mecja G, Muntwyler S, Nestorova A, Huang T, Sakar MS, Grossniklaus U, Nelson BJ (2015b) Real-time automated characterization of 3D morphology and mechanics of developing plant cells. Int J Rob Res 34:1136–1146Google Scholar
  26. Ferguson BA, Dreisbach TA, Parks CG, Filip GM, Schmitt CL (2003) Coarse-scale population structure of pathogenic Armillaria species in a mixed-conifer forest in the Blue Mountains of northeast Oregon. Can J For Res 33:612–623CrossRefGoogle Scholar
  27. Fernandes A, Chen X, Scotchford C, Walker J, Wells D, Roberts C, Everitt N (2012) Mechanical properties of epidermal cells of whole living roots of Arabidopsis thaliana: an atomic force microscopy study. Phys Rev E 85:021,916CrossRefGoogle Scholar
  28. Flintham JE, Börner A, Worland AJ, Gale MD (1997) Optimizing wheat grain yield: effects of Rht (gibberellin-insensitive) dwarfing genes. J Agric Sci 128:11–25CrossRefGoogle Scholar
  29. Forouzesh E, Goel A, Mackenzie SA, Turner JA (2013) In vivo extraction of Arabidopsis cell turgor pressure using nanoindentation in conjunction with finite element modeling. Plant J 73:509–520CrossRefPubMedGoogle Scholar
  30. Geitmann A, Parre E (2004a) The local cytomechanical properties of growing pollen tubes correspond to the axial distribution of structural cellular elements. Sex Plant Reprod 17:9–16Google Scholar
  31. Geitmann A, Parre E (2004b) The local cytomechanical properties of growing pollen tubes correspond to the axial distribution of structural cellular elements. Sex Plant Reprod 17:9–16Google Scholar
  32. Geitmann A, McConnaughey W, Lang-Pauluzzi I, Franklin-Tong VE, Emons AMC (2004) Cytomechanical properties of Papaver pollen tubes are altered after self-incompatibility challenge. Biophys J 86:3314–3323CrossRefPubMedPubMedCentralGoogle Scholar
  33. Geng T, Bredeweg EL, Szymanski CJ, Liu B, Baker SE, Orr G, Evans JE, Kelly RT (2015) Compartmentalized microchannel array for high-throughput analysis of single cell polarized growth and dynamics. Sci Rep 5:16,111CrossRefGoogle Scholar
  34. Gossot O, Geitmann A (2007) Pollen tube growth: coping with mechanical obstacles involves the cytoskeleton. Planta 226:405–416CrossRefPubMedGoogle Scholar
  35. Green PB (1968) Growth physics in Nitella: a method for continuous in vivo analysis of extensibility based on a micro-manometer technique for turgor pressure. Plant Physiol 43:1169–1184CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168CrossRefGoogle Scholar
  37. Heilbronn A (1914) Zustand des Plasmas und Reizbarkeit. Ein Beitrag zur Physiologie der lebenden Substanz. Jahrb wiss Botan 54:357–390Google Scholar
  38. Ho JC, Ueda J, Shimizu T (2016) The impact of mechanical stress on stem cell properties: the link between cell shape and pluripotency. Histol Histopathol 31:41–50PubMedGoogle Scholar
  39. Hülskamp M, Schneitz K, Pruitt R (1995) Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7:57–64CrossRefPubMedPubMedCentralGoogle Scholar
  40. Husken D, Steudle E, Zimmermann U (1978) Pressure probe technique for measuring water relations of cells in higher plants. Plant Physiol 61:158–163CrossRefPubMedPubMedCentralGoogle Scholar
  41. Jauh GY, Lord EM (1996) Localization of pectins and arabinogalactan-proteins in lily (Lilium longiflorum L.) pollen tube and style, and their possible roles in pollination. Planta 199:251–261CrossRefGoogle Scholar
  42. Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kailas L, Ratcliffe E, Hayhurst E, Walker M, Foster S, Hobbs J (2009) Immobilizing live bacteria for AFM imaging of cellular processes. Ultramicroscopy 109:775–780CrossRefPubMedGoogle Scholar
  44. Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM (2003) Chemocyanin a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100:16,125–16,130CrossRefGoogle Scholar
  45. Kim MS, Pratt JR, Brand U, Jones CW (2011) Report on the first international comparison of small force facilities: a pilot study at the micronewton level. Metrologia 49:70–81CrossRefGoogle Scholar
  46. Lesniewska E, Adrian M, Klinguer A, Pugin A (2004) Cell wall modification in grapevine cells in response to UV stress investigated by atomic force microscopy. Ultramicroscopy 100:171–178CrossRefPubMedGoogle Scholar
  47. Lintilhac PM, Wei C, Tanguay JJ, Outwater JO (2000) Ball tonometry: a rapid, nondestructive method for measuring cell turgor pressure in thin-walled plant cells. J Plant Growth Regul 19:90–97CrossRefPubMedGoogle Scholar
  48. Lord EM, Kohorn LU (1986) Gynoecial development, pollination, and the path of pollen tube growth in the tepary bean, Phaseolus acutifolius. Am J Bot 73:70–78CrossRefGoogle Scholar
  49. Luu DT, Marty-Mazars D, Trick M, Dumas C, Heizmann P (1999) Pollen-stigma adhesion in Brassica spp involves SLG and SLR1 glycoproteins. Plant Cell 11:251–262PubMedPubMedCentralGoogle Scholar
  50. Messerli MA, Robinson KR (2003) Ionic and osmotic disruptions of the lily pollen tube oscillator: testing proposed models. Planta 217:147–57PubMedGoogle Scholar
  51. Milani P, Gholamirad M, Traas J, Arnéodo A, Boudaoud A, Argoul F, Hamant O (2011) In vivo analysis of local wall stiffness at the shoot apical meristem in Arabidopsis using atomic force microscopy. Plant J 67:1116–1123CrossRefPubMedGoogle Scholar
  52. Miyoshi M (1895) Die Durchbohrung von Membranen durch Pilzfäden. Jahrb Wissensch Bot 28:269–289Google Scholar
  53. Mollet JC, Park SY, Nothnagel EA, Lord EM (2000) A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12:1737–1750CrossRefPubMedPubMedCentralGoogle Scholar
  54. Mollet JC, Leroux C, Dardelle F, Lehner A (2013) Cell wall composition biosynthesis and remodeling during pollen tube growth. Plants 2:107–147CrossRefPubMedPubMedCentralGoogle Scholar
  55. Money NP (2007) Biomechanics of invasive hyphal growth. In: Howard RJ, Gow NAR (eds) Biology of the fungal cell. Springer, Berlin/Heidelberg, pp 237–249CrossRefGoogle Scholar
  56. Muntwyler S, Beyeler F, Nelson BJ (2009) Three-axis micro-force sensor with sub-micro-newton measurement uncertainty and tunable force range. J Micromech Microeng 20:025,011CrossRefGoogle Scholar
  57. Nagelkerke A, Bussink J, Rowan AE, Span P (2015) The mechanical microenvironment in cancer: how physics affects tumours. Semin Cancer Biol 35:62–70CrossRefPubMedGoogle Scholar
  58. Ng L, Hung HH, Sprunt A, Chubinskaya S, Ortiz C, Grodzinsky A (2007) Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix. J Biomech 40:1011–1023CrossRefPubMedGoogle Scholar
  59. Nili A, Yi H, Crespi VH, Puri VM (2015) Examination of biological hotspot hypothesis of primary cell wall using a computational cell wall network model. Cellulose 22:1027–1038CrossRefGoogle Scholar
  60. Nilsson J, Evander M, Hammarström B, Laurell T (2009) Review of cell and particle trapping in microfluidic systems. Anal Chim Acta 649:141–157CrossRefPubMedGoogle Scholar
  61. Nye PH (1966) The effect of the nutrient intensity and buffering power of a soil and the absorbing power, size and root hairs of a root, on nutrient absorption by diffusion. Plant Soil 25:81–105CrossRefGoogle Scholar
  62. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361CrossRefPubMedGoogle Scholar
  63. Palanivelu R, Preuss D (2006) Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 6:7CrossRefPubMedPubMedCentralGoogle Scholar
  64. Park SY, Jauh GY, Mollet JC, Eckard KJ, Nothnagel EA, Walling LL, Lord EM (2000) A lipid transfer-like protein is necessary for lily pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12:151–164CrossRefPubMedPubMedCentralGoogle Scholar
  65. Park YB, Cosgrove DJ (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158:1933–1943CrossRefPubMedPubMedCentralGoogle Scholar
  66. Parre E, Geitmann A (2005a) More than a leak sealant. The mechanical properties of callose in pollen tubes. Plant Physiol 137:274–286Google Scholar
  67. Parre E, Geitmann a (2005b) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592Google Scholar
  68. Pauly M, Albersheim P, Darvill A, York WS (1999) Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. Plant J 20:629–639CrossRefPubMedGoogle Scholar
  69. Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Höfte H (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol 21:1720–1726CrossRefPubMedGoogle Scholar
  70. Pérez-de-Luque A (2013) Haustorium invasion into host tissues. In: Parasitic Orobanchaceae. Springer Science + Business Media, New York, pp 75–86CrossRefGoogle Scholar
  71. Pertl H, Pockl M, Blaschke C, Obermeyer G (2010) Osmoregulation in Lilium pollen grains occurs via modulation of the plasma membrane H+ ATPase activity by 14-3-3 proteins. Plant Physiol 154:1921–1928Google Scholar
  72. Radotic K, Roduit C, Simonovic J, Hornitschek P, Fankhauser C, Mutavdzic D, Steinbach G, Dietler G, Kasas S (2012) Atomic force microscopy stiffness tomography on living Arabidopsis thaliana cells reveals the mechanical properties of surface and deep cell-wall layers during growth. Biophys J 103:386–394CrossRefPubMedPubMedCentralGoogle Scholar
  73. Rae AL, Harris PJ, Bacic A, Clarke AE (1985) Composition of the cell walls of Nicotiana alata Link et Otto pollen tubes. Planta 166:128–133CrossRefPubMedGoogle Scholar
  74. 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 166:139–151CrossRefPubMedPubMedCentralGoogle Scholar
  75. Routier-Kierzkowska AL, Smith RS (2013) Measuring the mechanics of morphogenesis. Curr Opin Plant Biol 16:25–32CrossRefPubMedGoogle Scholar
  76. Routier-Kierzkowska AL, Weber A, Kochova P, Felekis D, Nelson BJ, Kuhlemeier C, Smith RS (2012) Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiol 158:1514–1522CrossRefPubMedPubMedCentralGoogle Scholar
  77. Sanati Nezhad A, Naghavi M, Packirisamy M, Bhat R, Geitmann A (2013) Quantification of cellular penetrative forces using lab-on-a-chip technology and finite element modeling. Proc Natl Acad Sci USA 110:8093–8098CrossRefPubMedPubMedCentralGoogle Scholar
  78. Saunders CS, Yang SY, Eun JS, Feuz DM, ZoBell DR (2015) Feeding a brown midrib corn silage-based diet to growing beef steers improves growth performance and economic returns. Can J Anim Sci Can J Anim Sci 95:625–631CrossRefGoogle Scholar
  79. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289CrossRefPubMedGoogle Scholar
  80. Schlupmann H, Bacic A, Read SM (1994) Uridine diphosphate glucose metabolism and callose synthesis in cultured pollen tubes of Nicotiana alata Link et Otto. Plant Physiol 105:659–670CrossRefPubMedPubMedCentralGoogle Scholar
  81. Shamsudhin N, Atakan HB, Läubli N, Vogler H, Hu C, Sebastian A, Grossniklaus U, Nelson BJ (2016a) Probing the micromechanics of the fastest growing plant cell – the pollen tube. In: Proceedings in IEEE International Conference on Engineering in Medicine and Biology (EMBC2016), Orlando, USAGoogle Scholar
  82. Shamsudhin N, Läubli N, Atakan HB, Vogler H, Hu C, Häberle W, Sebastian A, Grossniklaus U, Nelson BJ (2016b) Massively parallelized pollen tube guidance and mechanical measurements on a lab-on-a-chip platform. PLoS One 11:e0168138Google Scholar
  83. Shawky JH, Davidson LA (2015) Tissue mechanics and adhesion during embryo development. Dev Biol 401:152–64CrossRefPubMedGoogle Scholar
  84. Shimizu KK, Okada K (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127:4511–4518PubMedGoogle Scholar
  85. Smith ML, Bruhn JN, Anderson JB (1992) The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428–431CrossRefGoogle Scholar
  86. Sniadecki NJ, Anguelouch A, Yang MT, Lamb CM, Liu Z, Kirschner SB, Liu Y, Reich DH, Chen CS (2007) Magnetic microposts as an approach to apply forces to living cells. Proc Natl Acad Sci USA 104:14,553–14,558CrossRefGoogle Scholar
  87. Sun Y, Wan KT, Roberts KP, Bischof JC, Nelson BJ (2003) Mechanical property characterization of mouse zona pellucida. IEEE Trans Nanobiosci 2:279–286CrossRefGoogle Scholar
  88. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL (2005) A microfluidic culture platform for CNS axonal injury regeneration and transport. Nat Methods 2:599–605CrossRefPubMedPubMedCentralGoogle Scholar
  89. Tomos AD, Leigh RA (1999) The pressure probe: a versatile tool in plant cell physiology. Annu Rev Plant Physiol Plant Mol Biol 50:447–472CrossRefPubMedGoogle Scholar
  90. Vanderwerff L, Ferraretto L, Shaver R (2015) Brown midrib corn shredlage in diets for high-producing dairy cows. J Dairy Sci 98:5642–5652CrossRefPubMedGoogle Scholar
  91. 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 73:617–627CrossRefPubMedGoogle Scholar
  92. de Vries H (1884) Eine Methode zur Analyse der Turgorkraft. Bernstein, BerlinGoogle Scholar
  93. Weber A, Braybrook S, Huflejt M, Mosca G, Routier-Kierzkowska AL, Smith RS (2015) Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments. J Exp Bot 66:3229–3241CrossRefPubMedPubMedCentralGoogle Scholar
  94. Wei C (2001) An insight into cell elasticity and load-bearing ability. Measurement and theory. Plant Physiol 126:1129–1138CrossRefPubMedPubMedCentralGoogle Scholar
  95. Wright GD, Arlt J, Poon WC, Read ND (2007) Optical tweezer micromanipulation of filamentous fungi. Fungal Genet Biol 44:1–13CrossRefPubMedGoogle Scholar
  96. Wu J, Lin Y, Zhang XL, Pang DW, Zhao J (2008) IAA stimulates pollen tube growth and mediates the modification of its wall composition and structure in Torenia fournieri. J Exp Bot 59:2529–2543CrossRefPubMedPubMedCentralGoogle Scholar
  97. Yarbrough JM, Himmel ME, Ding SY (2009) Plant cell wall characterization using scanning probe microscopy techniques. Biotechnol Biofuels 2:17CrossRefPubMedPubMedCentralGoogle Scholar
  98. Yetisen AK, Jiang L, Cooper JR, Qin Y, Palanivelu R, Zohar Y (2011) A microsystem-based assay for studying pollen tube guidance in plant reproduction. J Micromech Microeng 21:054,018CrossRefGoogle Scholar
  99. Yoshida S, Cui S, Ichihashi Y, Shirasu K (2016) The haustorium, a specialized invasive organ in parasitic plants. Annu Rev Plant Biol 67:643–667CrossRefPubMedGoogle Scholar
  100. Zamir EA, Taber LA (2004) On the effects of residual stress in microindentation tests of soft tissue structures. J Biomech Eng 126:276–283CrossRefPubMedGoogle Scholar
  101. Zerzour R, Kroeger J, Geitmann A (2009) Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev Biol 334:437–446CrossRefPubMedGoogle Scholar
  102. Zhang T, Zheng Y, Cosgrove DJ (2016) Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy. Plant J 85:179–192CrossRefPubMedGoogle Scholar
  103. Zhao Z, Crespi VH, Kubicki JD, Cosgrove DJ, Zhong L (2014) Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation. Cellulose 21:1025–1039CrossRefGoogle Scholar
  104. Zonia L, Munnik T (2008) Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J Exp Bot 59:861–873CrossRefPubMedGoogle Scholar
  105. Zonia L, Müller M, Munnik T (2006) Hydrodynamics and cell volume oscillations in the pollen tube apical region are integral components of the biomechanics of Nicotiana tabacum pollen tube growth. Cell Biochem Biophys 46:209–232CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Plant and Microbial Biology and Zurich-Basel Plant Science CenterUniversity of ZurichZurichSwitzerland
  2. 2.Multi-Scale Robotics LabETH ZurichZurichSwitzerland

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