How to shape a cylinder: pollen tube as a model system for the generation of complex cellular geometry

Expansive growth in plant cells is a formidable problem for biophysical studies, and the mechanical principles governing the generation of complex cellular geometries are still poorly understood. Pollen, the male gametophyte stage of the flowering plants, is an excellent model system for the investigation of the mechanics of complex growth processes. The initiation of pollen tube growth requires first of all, the spatially confined formation of a protuberance. This process must be controlled by the mechanical properties of the cell wall, since turgor is a non-vectorial force. In the elongating tube, cell wall expansion is confined to the apex of the cell, requiring the tubular region to be stabilized against turgor-induced tensile stress. Tip focused surface expansion must be coordinated with the supply of cell wall material to this region requiring the precise, logistical control of intracellular transport processes. The advantage of such a demanding mechanism is the high efficiency it confers on the pollen tube in leading an invasive way of life.

[1]  Daphne Preuss,et al.  Pollen and Stigma Structure and Function: The Role of Diversity in Pollination , 2004, The Plant Cell Online.

[2]  Johnw . Anderson,et al.  2,6-Dichlorobenzonitrile, a cellulose biosynthesis inhibitor, affects morphology and structural integrity of petunia and lily pollen tubes , 2002 .

[3]  J. Skvarla,et al.  The elasticity of the exine , 2000 .

[4]  E. Pacini Harmomegathic characters of Pteridophyta spores and Spermatophyta pollen , 1990 .

[5]  V. Polito,et al.  Spatial and temporal organization of actin during hydration, activation, and germination of pollen inPyrus communis L.: a population study , 1988, Protoplasma.

[6]  Pollen tube growth: coping with mechanical obstacles involves the cytoskeleton , 2007, Planta.

[7]  A. Witztum,et al.  Phototactic chloroplast displacement in the photosynthetic mutant, Lemna paucicostata strain 1073. , 1979 .

[8]  W. W. Payne Observations of Harmomegathy in Pollen of Anthophyta , 1972 .

[9]  M. Sassen FINE STRUCTURE OF PETUNIA POLLEN GRAIN AND POLLEN TUBE , 1964 .

[10]  J. Muller Form and Function in Angiosperm Pollen , 1979 .

[11]  T. Baskin,et al.  Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube , 2005, Planta.

[12]  C. A. Pell,et al.  Mechanical Design of Fiber-Wound Hydraulic Skeletons: The Stiffening and Straightening of Embryonic Notochords1 , 2000 .

[13]  W. Vensel,et al.  Proteome mapping of mature pollen of Arabidopsis thaliana , 2005, Proteomics.

[14]  J. Heslop-Harrison,et al.  Pollen-wall proteins: localization and enzymic activity. , 1970, Journal of cell science.

[15]  L. Vidali,et al.  Actin polymerization is essential for pollen tube growth. , 2001, Molecular biology of the cell.

[16]  J. Dumais,et al.  Not-so-tip-growth , 2009, Plant signaling & behavior.

[17]  Thomas Rausch,et al.  Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. , 2008, The Plant journal : for cell and molecular biology.

[18]  M. Cresti,et al.  Pollen Germination and Pollen Tube Growth , 2001 .

[19]  J. S. Heslop-Harrison,et al.  AN INTERPRETATION OF THE HYDRODYNAMICS OF POLLEN , 1979 .

[20]  M. Suárez-Cervera,et al.  Regular Papers / Articles OrdinairesIntine wall modifications during germination of Zygophyllum fabago (Zygophyllaceae) pollen grains , 2003 .

[21]  M. Cresti,et al.  ULTRASTRUCTURE OF NICOTIANA ALATA POLLEN, ITS GERMINATION AND EARLY TUBE FORMATION , 1985 .

[22]  N. Carpita,et al.  Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. , 1993, The Plant journal : for cell and molecular biology.

[23]  A. Geitmann,et al.  Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy (STICS) and fluorescence recovery after photobleaching (FRAP) , 2008 .

[24]  E. Arcalis,et al.  Pectin distribution pattern in the apertural intine of Euphorbia peplus L. (Euphorbiaceae) pollen , 2001, Sexual Plant Reproduction.

[25]  F. Harold,et al.  Force and compliance: rethinking morphogenesis in walled cells. , 2002, Fungal genetics and biology : FG & B.

[26]  Charles R Steele,et al.  An anisotropic-viscoplastic model of plant cell morphogenesis by tip growth. , 2006, The International journal of developmental biology.

[27]  J. Boyer,et al.  Calcium pectate chemistry controls growth rate of Chara corallina. , 2006, Journal of experimental botany.

[28]  A. G. Klein,et al.  Tip growth in plant cells may be amoeboid and not generated by turgor pressure , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  E. S. Castle THE TOPOGRAPHY OF TIP GROWTH IN A PLANT CELL , 1958, The Journal of general physiology.

[30]  M. Cresti,et al.  Germination and early tube development in vitro of Lycopersicum peruvianum pollen: Ultrastructural features , 2004, Planta.

[31]  M. Braun,et al.  Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. , 2000, Developmental biology.

[32]  I. Lichtscheidl,et al.  Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis , 1995, Protoplasma.

[33]  D. Cosgrove,et al.  Class B β-expansins are needed for pollen separation and stigma penetration , 2009, Sexual Plant Reproduction.

[34]  S. Gilroy,et al.  Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. , 1998, Development.

[35]  Anja Geitmann,et al.  Microfilament orientation constrains vesicle flow and spatial distribution in growing pollen tubes. , 2009, Biophysical journal.

[36]  M. Suárez-Cervera,et al.  Allergenic and antigenic proteins released in the apertural sporoderm during the activation process in grass pollen grains , 1997, Sexual Plant Reproduction.

[37]  C. Clément,et al.  Anther and pollen : from biology to biotechnology , 1999 .

[38]  A. Kapp,et al.  Actin polymerization. , 2000, Methods in molecular biology.

[39]  A. Geitmann,et al.  More Than a Leak Sealant. The Mechanical Properties of Callose in Pollen Tubes1 , 2005, Plant Physiology.

[40]  A. Bacic,et al.  Composition of the cell walls of Nicotiana alata Link et Otto pollen tubes , 1985, Planta.

[41]  Rui Malhó,et al.  The pollen tube : a cellular and molecular perspective , 2006 .

[42]  M. Nepi,et al.  What may be the significance of polysiphony in Lavatera arborea , 1999 .

[43]  M. Bolick Mechanics as an aid to interpreting pollen structure and function , 1981 .

[44]  Anja Geitmann,et al.  Magnitude and Direction of Vesicle Dynamics in Growing Pollen Tubes Using Spatiotemporal Image Correlation Spectroscopy and Fluorescence Recovery after Photobleaching1[W][OA] , 2008, Plant Physiology.

[45]  D. Cosgrove,et al.  Regulation of Root Hair Initiation and Expansin Gene Expression in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006437. , 2002, The Plant Cell Online.

[46]  N. P. Money Wishful Thinking of Turgor Revisited: The Mechanics of Fungal Growth , 1997 .

[47]  Jacques Dumais,et al.  The Mechanics of Surface Expansion Anisotropy in Medicago truncatula Root Hairs1 , 2004, Plant Physiology.

[48]  W. W. Payne Structure and function in angiosperm pollen wall evolution , 1981 .

[49]  M. Lenartowska,et al.  Actin filament organization and polarity in pollen tubes revealed by myosin II subfragment 1 decoration , 2008, Planta.

[50]  M. D. Lazzaro,et al.  Disruption of cellulose synthesis by isoxaben causes tip swelling and disorganizes cortical microtubules in elongating conifer pollen tubes , 2003, Protoplasma.

[51]  J. Verbelen,et al.  Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. , 2001, Plant physiology.

[52]  F. Harold,et al.  Extension growth of the water mold Achlya: interplay of turgor and wall strength. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Y. Chebli,et al.  Morphogenesis of complex plant cell shapes: the mechanical role of crystalline cellulose in growing pollen tubes , 2010, Sexual Plant Reproduction.

[54]  E. M. Meyerowitz,et al.  Arabidopsis thaliana , 2022, CABI Compendium.

[55]  A. Geitmann,et al.  Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. , 2009, Developmental biology.

[56]  Eric J. Pedersen,et al.  Dynamics of protein expression during pollen germination in canola (Brassica napus) , 2009, Planta.

[57]  Peter K Hepler,et al.  Pectin Methylesterase, a Regulator of Pollen Tube Growth1[w] , 2005, Plant Physiology.

[58]  T. Baskin Anisotropic expansion of the plant cell wall. , 2005, Annual review of cell and developmental biology.

[59]  V. Citovsky,et al.  Pollen-specific pectin methylesterase involved in pollen tube growth. , 2006, Developmental biology.

[60]  P. Bhalla,et al.  Transcriptome-based examination of putative pollen allergens of rice (Oryza sativa ssp. japonica). , 2008, Molecular plant.

[61]  R. Panstruga,et al.  A reference map of the Arabidopsis thaliana mature pollen proteome. , 2005, Biochemical and biophysical research communications.

[62]  A. Geitmann,et al.  Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense , 2005, Planta.

[63]  T. Higashiyama,et al.  Gametophytic pollen tube guidance , 2008, Sexual Plant Reproduction.

[64]  M. Bolick,et al.  Breaking strengths of pollen grain walls , 2004, Plant Systematics and Evolution.

[65]  A. Geitmann,et al.  Mechanics and modeling of plant cell growth. , 2009, Trends in plant science.

[66]  I. Heath Preservation of a labile cortical array of actin filaments in growing hyphal tips of the fungus Saprolegnia ferax , 1987 .

[67]  J. Feijó,et al.  Gene Family Analysis of the Arabidopsis Pollen Transcriptome Reveals Biological Implications for Cell Growth, Division Control, and Gene Expression Regulation1[w] , 2005, Plant Physiology.

[68]  M. Mccully,et al.  The use of an optical brightener in the study of plant structure. , 1975, Stain technology.

[69]  J. S. Heslop-Harrison,et al.  Pollen Walls as Adaptive Systems , 1979 .

[70]  A. Huang,et al.  Maize Pollen Coat Xylanase Facilitates Pollen Tube Penetration into Silk during Sexual Reproduction* , 2007, Journal of Biological Chemistry.

[71]  J. Heslop-Harrison,et al.  Germination of Monocolpate Angiosperm Pollen: Evolution of the Actin Cytoskeleton and Wall during Hydration, Activation and Tube Emergence , 1992 .

[72]  Calcium pectate chemistry controls growth rate of , 2006 .

[73]  Tai Wang,et al.  Proteomics Identification of Differentially Expressed Proteins Associated with Pollen Germination and Tube Growth Reveals Characteristics of Germinated Oryza sativa Pollen*S , 2007, Molecular & Cellular Proteomics.

[74]  Tension required for pectate chemistry to control growth in Chara corallina. , 2007, Journal of experimental botany.

[75]  Anja Geitmann,et al.  The local cytomechanical properties of growing pollen tubes correspond to the axial distribution of structural cellular elements , 2004, Sexual Plant Reproduction.

[76]  E. Friedberg The Molecular Biology of Nucleotide Excision Repair of DNA: Recent Progress , 1987, Journal of Cell Science.

[77]  J. Derksen,et al.  The wall ofPinus sylvestris L. pollen tubes , 1999, Protoplasma.

[78]  R. Benkert,et al.  The turgor pressure of growing lily pollen tubes , 1997, Protoplasma.

[79]  G. Bollinger,et al.  Population Study , 2020, Definitions.

[80]  F. Harold,et al.  Two water molds can grow without measurable turgor pressure , 1993, Planta.

[81]  P. Hepler,et al.  Enforced growth-rate fluctuation causes pectin ring formation in the cell wall of Lilium longiflorum pollen tubes , 1996, Planta.