How pollen tubes grow.

Sexual reproduction of flowering plants depends on delivery of the sperm to the egg, which occurs through a long, polarized projection of a pollen cell, called the pollen tube. The pollen tube grows exclusively at its tip, and this growth is distinguished by very fast rates and reaches extended lengths. Thus, one of the most fascinating aspects of pollen biology is the question of how enough cell wall material is produced to accommodate such rapid extension of pollen tube, and how the cell wall deposition and structure are regulated to allow for rapid changes in the direction of growth. This review discusses recent advances in our understanding of the mechanism of pollen tube growth, focusing on such basic cellular processes as control of cell shape and growth by a network of cell wall-modifying enzymes, molecular motor-mediated vesicular transport, and intracellular signaling by localized gradients of second messengers.

[1]  A. Geitmann,et al.  Immunogold localization of arabinogalactan proteins, unesterified and esterified pectins in pollen grains and pollen tubes ofNicotiana tabacum L. , 1995, Protoplasma.

[2]  M. Hoyt Cellular roles of kinesin and related proteins. , 1994, Current opinion in cell biology.

[3]  M. Hawes,et al.  Effect of Pectin Methylesterase Gene Expression on Pea Root Development , 1999, Plant Cell.

[4]  D. Oppenheimer,et al.  Extragenic suppressors of the arabidopsis zwi-3 mutation identify new genes that function in trichome branch formation and pollen tube growth. , 1999, Development.

[5]  A. Bacic,et al.  Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum , 1998, Planta.

[6]  Zhenbiao Yang,et al.  The Rop GTPase: an emerging signaling switch in plants , 2000, Plant Molecular Biology.

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

[8]  L. Vidali,et al.  Polarized cell growth in higher plants. , 2001, Annual review of cell and developmental biology.

[9]  Peter K Hepler,et al.  Pectin Methylesterases and Pectin Dynamics in Pollen Tubes , 2005, The Plant Cell Online.

[10]  K. Feldmann,et al.  Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[12]  D. J. Lewandowski,et al.  Genetics and expression of two pectinesterase genes in Valencia orange , 1998 .

[13]  N. Hirokawa,et al.  Kinesin and dynein superfamily proteins and the mechanism of organelle transport. , 1998, Science.

[14]  M. Steer,et al.  Pollen tube tip growth. , 1989, The New phytologist.

[15]  T. Brembu,et al.  Genetic structure and evolution of RAC-GTPases in Arabidopsis thaliana. , 2000, Genetics.

[16]  G. Cai,et al.  An immunoreactive homolog of mammalian kinesin in Nicotiana tabacum pollen tubes. , 1992, Cell motility and the cytoskeleton.

[17]  P. K. Hepler,et al.  Fluorescence microscopic localization of actin in pollen tubes: comparison of actin antibody and phalloidin staining. , 1989, Cell motility and the cytoskeleton.

[18]  S. Pfeffer,et al.  Rab GTPases, Directors of Vesicle Docking* , 1998, The Journal of Biological Chemistry.

[19]  R. Pressey Role of Pectinesterase in pH-Dependent Interactions between Pea Cell Wall Polymers. , 1984, Plant physiology.

[20]  G. Cai,et al.  Kinesin-related polypeptide is associated with vesicles from Corylus avellana pollen. , 1994, Cell motility and the cytoskeleton.

[21]  V. Citovsky,et al.  Systemic movement of a tobamovirus requires host cell pectin methylesterase. , 2003, The Plant journal : for cell and molecular biology.

[22]  Jian Huang,et al.  An Ankyrin Repeat-Containing Protein, Characterized as a Ubiquitin Ligase, Is Closely Associated with Membrane-Enclosed Organelles and Required for Pollen Germination and Pollen Tube Growth in Lily1[W] , 2006, Plant Physiology.

[23]  F. Nagy,et al.  Characterization of Membrane-Bound Small GTP-Binding Proteins from Nicotiana tabacum , 1995, Plant physiology.

[24]  A. Reddy,et al.  A Novel Plant Calmodulin-binding Protein with a Kinesin Heavy Chain Motor Domain (*) , 1996, The Journal of Biological Chemistry.

[25]  F. Micheli Pectin methylesterases: cell wall enzymes with important roles in plant physiology. , 2001, Trends in plant science.

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

[27]  V. Olkkonen,et al.  Role of Rab GTPases in membrane traffic. , 1997, International review of cytology.

[28]  J. Mollet,et al.  Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Gross,et al.  Free Ca2+ Gradient in Growing Pollen Tubes of Lillium , 1992 .

[30]  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.

[31]  K. Skryabin,et al.  Role of the leader sequence in tobacco pectin methylesterase secretion , 2006, FEBS letters.

[32]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[33]  L. Vidali,et al.  Actin and pollen tube growth , 2005, Protoplasma.

[34]  G. Cai,et al.  The kinesin-immunoreactive homologue from Nicotiana tabacum pollen tubes: Biochemical properties and subcellular localization , 1993, Planta.

[35]  L. Vidali,et al.  The Regulation of Actin Organization by Actin-Depolymerizing Factor in Elongating Pollen Tubes Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003038. , 2002, The Plant Cell Online.

[36]  Identification and Characterization of Stretch-Activated Ion Channels in Pollen Protoplasts 1 , 2004 .

[37]  M. Raudaskoski,et al.  Role of microtubules in the movement of the vegetative nucleus and generative cell in tobacco pollen tubes , 1995, Sexual Plant Reproduction.

[38]  U. Kristen,et al.  Microtubules are involved in maintaining the cellular polarity in pollen tubes ofNicotiana sylvestris , 1994, Protoplasma.

[39]  Zhenbiao Yang,et al.  Control of Pollen Tube Tip Growth by a Rop GTPase–Dependent Pathway That Leads to Tip-Localized Calcium Influx , 1999, Plant Cell.

[40]  L. Camardella,et al.  Kiwi protein inhibitor of pectin methylesterase , 2000 .

[41]  L. Tao,et al.  Regulation of pollen tube growth by Rac‐like GTPases , 2003 .

[42]  T. Deguchi,et al.  Stimulation of phosphatidic acid of calcium influx and cyclic GMP synthesis in neuroblastoma cells. , 1981, The Journal of biological chemistry.

[43]  M. Wakelam,et al.  The regulation of phospholipase D by inositol phospholipids and small GTPases , 2002, FEBS letters.

[44]  M. Steer,et al.  Membrane recycling and the control of secretory activity in pollen tubes. , 1983, Journal of cell science.

[45]  G. Cai,et al.  Cytoskeletal Basis of Organelle Trafficking in the Angiosperm Pollen Tube , 2000 .

[46]  V. Rybin,et al.  Two distinct effectors of the small GTPase Rab5 cooperate in endocytic membrane fusion , 1998, The EMBO journal.

[47]  B. Paschal,et al.  Regulation of nuclear import and export by the GTPase Ran. , 2002, International review of cytology.

[48]  L. Wolpert Developmental Biology , 1968, Nature.

[49]  Zhenbiao Yang,et al.  Analysis of the Small GTPase Gene Superfamily of Arabidopsis1 , 2003, Plant Physiology.

[50]  J. Feijó,et al.  Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx Is Delayed. , 1997, The Plant cell.

[51]  D. Kovar,et al.  Latrunculin B Has Different Effects on Pollen Germination and Tube Growth , 1999, Plant Cell.

[52]  V. Citovsky,et al.  Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell‐to‐cell movement , 2000, The EMBO journal.

[53]  J. Bamburg,et al.  Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases. , 2000, Journal of neurobiology.

[54]  A. Trewavas,et al.  Role of cytosolic free calcium in the reorientation of pollen tube growth , 1994 .

[55]  M. Cresti,et al.  Ultrastructure of the cytoskeleton in freeze-substituted pollen tubes ofNicotiana alata , 1987, Protoplasma.

[56]  G. Cai,et al.  In Vitro Assays Demonstrate That Pollen Tube Organelles Use Kinesin-Related Motor Proteins to Move along Microtubules Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.005645. , 2003, The Plant Cell Online.

[57]  Hong Wang,et al.  A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth , 1995, Cell.

[58]  K. Rathore,et al.  A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. , 1991, Developmental biology.

[59]  A. Giovane,et al.  A glycoprotein inhibitor of pectin methylesterase in kiwi fruit (Actinidia chinensis). , 1990, European journal of biochemistry.

[60]  R. Brown,et al.  Cellulose synthases and related enzymes. , 2000, Current opinion in plant biology.

[61]  M. Cresti,et al.  Cytoskeletal Elements, Cell Shaping and Movement in the Angiosperm Pollen Tube , 1988 .

[62]  D. McCormick,et al.  Essential Role of Phosphoinositide Metabolism in Synaptic Vesicle Recycling , 1999, Cell.

[63]  I. Moore,et al.  The Arabidopsis Rab GTPase family: another enigma variation. , 2002, Current opinion in plant biology.

[64]  T F Martin,et al.  Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. , 1998, Annual review of cell and developmental biology.

[65]  J. P. Mascarenhas Molecular Mechanisms of Pollen Tube Growth and Differentiation. , 1993, The Plant cell.

[66]  R. Vallee,et al.  DYNEINS: molecular structure and cellular function. , 1994, Annual review of cell biology.

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

[68]  D. Callaham,et al.  Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. , 1994, The Plant cell.

[69]  T. Schroer,et al.  Membrane motors. , 1999, Current opinion in cell biology.

[70]  C. Zuchowski,et al.  Chromosomal rearrangements which affect the chromosomal integration of the ribosomal genes in drosophila melanogaster , 1977, Cell.

[71]  Rajiv Dutta,et al.  Identification and Characterization of Stretch-Activated Ion Channels in Pollen Protoplasts1 , 2004, Plant Physiology.

[72]  S. Gilroy,et al.  Calcium-Dependent Protein Kinase Isoforms in Petunia Have Distinct Functions in Pollen Tube Growth, Including Regulating Polarity[W] , 2006, The Plant Cell Online.

[73]  J. Pereira-Leal,et al.  Evolution of the Rab family of small GTP-binding proteins. , 2001, Journal of molecular biology.

[74]  A. Orellana,et al.  The catalytic site of the pectin biosynthetic enzyme alpha-1,4-galacturonosyltransferase is located in the lumen of the Golgi. , 2001, Plant physiology.

[75]  T. Munnik Phosphatidic acid: an emerging plant lipid second messenger. , 2001, Trends in plant science.

[76]  R. Malhó Role of 1,4,5-inositol triphosphate-induced Ca2+ release in pollen tube orientation , 1998, Sexual Plant Reproduction.

[77]  S. Assmann Cyclic AMP as a Second Messenger in Higher Plants (Status and Future Prospects) , 1995, Plant physiology.

[78]  U. Folkers,et al.  Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. , 1997, Development.

[79]  J. Feijó,et al.  Cellular oscillations and the regulation of growth: the pollen tube paradigm , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[80]  Imara Y. Perera,et al.  Inositol signaling and plant growth , 2000, Trends in plant science.

[81]  R. Malhó,et al.  Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes. , 2004, The Plant journal : for cell and molecular biology.

[82]  Rex A. Cole,et al.  Polarized growth: maintaining focus on the tip. , 2006, Current opinion in plant biology.

[83]  Seung Y. Rhee,et al.  High-Throughput Fluorescent Tagging of Full-Length Arabidopsis Gene Products in Planta1 , 2004, Plant Physiology.

[84]  K. Pfister,et al.  Distinct cytoplasmic dynein complexes are transported by different mechanisms in axons. , 2000, Biochimica et biophysica acta.

[85]  I. Meier Nucleocytoplasmic trafficking in plant cells. , 2005, International review of cytology.

[86]  Zhenbiao Yang,et al.  Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast. , 1998, Plant physiology.

[87]  E. Lord,et al.  The mechanisms of pollination and fertilization in plants. , 2002, Annual review of cell and developmental biology.

[88]  G. Bolwell Cyclic AMP, the reluctant messenger in plants. , 1995, Trends in biochemical sciences.

[89]  G. Obermeyer,et al.  Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. , 1991, European journal of cell biology.

[90]  R. Malhó,et al.  Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. , 2005, Journal of experimental botany.

[91]  P. K. Hepler,et al.  Microtubules and microfilaments are both responsible for pollen tube elongation in the coniferPicea abies (Norway spruce) , 2000, Protoplasma.

[92]  V. Sundaresan,et al.  VANGUARD1 Encodes a Pectin Methylesterase That Enhances Pollen Tube Growth in the Arabidopsis Style and Transmitting Tract , 2005, The Plant Cell Online.

[93]  A. Ray,et al.  Pollen tube guidance by the female gametophyte. , 1997, Development.

[94]  H. Jörnvall,et al.  Pectinesterase. The primary structure of the tomato enzyme. , 1986, European journal of biochemistry.

[95]  L. Goldstein,et al.  Going mobile: microtubule motors and chromosome segregation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[96]  A. Reddy,et al.  Interaction of Arabidopsis kinesin-like calmodulin-binding protein with tubulin subunits: modulation by Ca(2+)-calmodulin. , 1997, The Plant journal : for cell and molecular biology.

[97]  D. Callaham,et al.  Tip-localized calcium entry fluctuates during pollen tube growth. , 1996, Developmental biology.

[98]  Colin Brownlee,et al.  Exocytosis and Endocytosis , 1999, Plant Cell.

[99]  B. Henrissat,et al.  Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. , 2000, Plant physiology.

[100]  A. Geitmann,et al.  Alterations in the Actin Cytoskeleton of Pollen Tubes Are Induced by the Self-Incompatibility Reaction in Papaver rhoeas , 2000, Plant Cell.

[101]  Samuel P Hazen,et al.  Cellulose Synthase-Like Genes of Rice1 , 2002, Plant Physiology.

[102]  D. Delmer,et al.  Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[103]  Harald Stenmark,et al.  The Rab GTPase family , 2001, Genome Biology.

[104]  G. Cai,et al.  Identification and Characterization of a Novel Microtubule-Based Motor Associated with Membranous Organelles in Tobacco Pollen Tubes , 2000, Plant Cell.

[105]  T. Bisseling,et al.  The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug , 1999 .

[106]  A. Trewavas,et al.  Localized Apical Increases of Cytosolic Free Calcium Control Pollen Tube Orientation. , 1996, The Plant cell.

[107]  D. Preuss,et al.  Pollen Tube Growth and Guidance Is Regulated by POP2, an Arabidopsis Gene that Controls GABA Levels , 2003, Cell.

[108]  M. Bordenave Analysis of Pectin Methyl Esterases , 1996 .

[109]  Heping Yang,et al.  Is there more than one way to attract a pollen tube? , 2005, Trends in plant science.

[110]  Zhenbiao Yang,et al.  ROP/RAC GTPase: an old new master regulator for plant signaling. , 2004, Current opinion in plant biology.

[111]  Zhenbiao Yang,et al.  The Rop GTPase switch turns on polar growth in pollen , 2000 .

[112]  D. Preuss,et al.  Plotting a course: multiple signals guide pollen tubes to their targets. , 2002, Developmental cell.

[113]  C R Somerville,et al.  The cellulose synthase superfamily. , 2000, Plant physiology.

[114]  E. Onelli,et al.  Dynein heavy chain (DHC)‐related polypeptides during pollen tube growth , 2003, Cell biology international.

[115]  A. Kermode,et al.  An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. , 2000, Plant physiology.

[116]  G. Cai,et al.  High molecular weight polypeptides related to dynein heavy chains in Nicotiana tabacum pollen tubes. , 1995, Journal of cell science.

[117]  J. Heslop-Harrison,et al.  Myosin associated with the surfaces of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes , 1989 .

[118]  L. Catoire,et al.  Investigation of the Action Patterns of Pectinmethylesterase Isoforms through Kinetic Analyses and NMR Spectroscopy , 1998, The Journal of Biological Chemistry.

[119]  A. Giovane,et al.  A glycoprotein inhibitor of pectin methylesterase in kiwi fruit. Purification by affinity chromatography and evidence of a ripening-related precursor. , 1995, European journal of biochemistry.

[120]  S. Gilroy,et al.  Petunia Phospholipase C1 Is Involved in Pollen Tube Growth[W] , 2006, The Plant Cell Online.

[121]  L. Staehelin,et al.  The Plant Golgi Apparatus: Structure, Functional Organization and Trafficking Mechanisms , 1995 .

[122]  A. Carroll,et al.  Ca2+, Annexins, and GTP Modulate Exocytosis from Maize Root Cap Protoplasts , 1998, Plant Cell.

[123]  J. Denecke,et al.  The Endoplasmic Reticulum—Gateway of the Secretory Pathway , 1999, Plant Cell.

[124]  A. Cheung,et al.  Actin-Depolymerizing Factor Mediates Rac/Rop GTPase–Regulated Pollen Tube Growth Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007153. , 2003, The Plant Cell Online.

[125]  D. Preuss,et al.  Pollen tube targeting and axon guidance: parallels in tip growth mechanisms. , 2000, Trends in cell biology.

[126]  L. Vidali,et al.  Rab2 GTPase Regulates Vesicle Trafficking between the Endoplasmic Reticulum and the Golgi Bodies and Is Important to Pollen Tube Growth Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000836. , 2002, The Plant Cell Online.

[127]  J. Ricard,et al.  Pectin methylesterase, metal ions and plant cell-wall extension. The role of metal ions in plant cell-wall extension. , 1991, The Biochemical journal.

[128]  N. Chua,et al.  Rac Homologues and Compartmentalized Phosphatidylinositol 4, 5-Bisphosphate Act in a Common Pathway to Regulate Polar Pollen Tube Growth , 1999, The Journal of cell biology.

[129]  P. K. Hepler,et al.  POLLEN GERMINATION AND TUBE GROWTH. , 1997, Annual review of plant physiology and plant molecular biology.

[130]  M. Seabra,et al.  Controlling the location and activation of Rab GTPases. , 2004, Current opinion in cell biology.

[131]  T. Shimmen,et al.  Characterization of the translocator associated with pollen tube organelles , 1990, Protoplasma.

[132]  K. Shimizu,et al.  Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. , 2000, Development.

[133]  S. Scordilis,et al.  Immunochemical and immunocytochemical identification of a myosin heavy chain polypeptide in Nicotiana pollen tubes. , 1989, Journal of cell science.

[134]  P. Bedinger The remarkable biology of pollen. , 1992, The Plant cell.

[135]  G. Cai,et al.  Dynein heavy chain-related polypeptides are associated with organelles in pollen tubes of Nicotiana tabacum , 1998, Sexual Plant Reproduction.

[136]  Tetsuya Higashiyama,et al.  Pollen-tube guidance: beacons from the female gametophyte. , 2003, Current opinion in plant biology.

[137]  T. Holdaway-Clarke,et al.  Control of pollen tube growth: role of ion gradients and fluxes. , 2003, The New phytologist.

[138]  H. Vihinen,et al.  Movement of generative cell and vegetative nucleus in tobacco pollen tubes is dependent on microtubule cytoskeleton but independent of the synthesis of callose plugs , 2002, Sexual Plant Reproduction.

[139]  L. Tamm,et al.  Membrane fusion: a structural perspective on the interplay of lipids and proteins. , 2003, Current opinion in structural biology.

[140]  P. Hussey,et al.  cAMP acts as a second messenger in pollen tube growth and reorientation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[141]  Signalling pathways in pollen tube growth and reorientation. , 2000 .

[142]  N. Raikhel,et al.  The Specificity of Vesicle Trafficking: Coat Proteins and SNAREs , 1999, Plant Cell.

[143]  Marino Zerial,et al.  Rab proteins as membrane organizers , 2001, Nature Reviews Molecular Cell Biology.

[144]  H. Linskens,et al.  Plant Cell Wall Analysis , 1996, Modern Methods of Plant Analysis.

[145]  K. Levasseur,et al.  Rab11 GTPase-Regulated Membrane Trafficking Is Crucial for Tip-Focused Pollen Tube Growth in Tobaccow⃞ , 2005, The Plant Cell Online.

[146]  A. Reddy,et al.  In vitro motility of AtKCBP, a calmodulin-binding kinesin protein of Arabidopsis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[147]  G. Piperno,et al.  The light chain p28 associates with a subset of inner dynein arm heavy chains in Chlamydomonas axonemes. , 1995, Molecular biology of the cell.

[148]  H. Jörnvall,et al.  Disulfide bridges in tomato pectinesterase: Variations from pectinesterases of other species; conservation of possible active site segments , 1992, Protein science : a publication of the Protein Society.

[149]  S. Pfeffer,et al.  Targeting Rab GTPases to distinct membrane compartments , 2004, Nature Reviews Molecular Cell Biology.

[150]  Dyneins Motor on in Plants , 2002, Traffic.

[151]  Yu. L. Dorokhovb,et al.  A novel function for a ubiquitous plant enzyme pectin methylesterase : the host-cell receptor for the tobacco mosaic virus movement protein , 1999 .

[152]  J. Armstrong How do Rab proteins function in membrane traffic? , 2000, The international journal of biochemistry & cell biology.

[153]  Zhenbiao Yang,et al.  ROP Gtpase–Dependent Dynamics of Tip-Localized F-Actin Controls Tip Growth in Pollen Tubes , 2001, The Journal of cell biology.

[154]  G. Piperno,et al.  ida4-1, ida4-2, and ida4-3 are intron splicing mutations affecting the locus encoding p28, a light chain of Chlamydomonas axonemal inner dynein arms. , 1995, Molecular biology of the cell.

[155]  J. Muschietti,et al.  Pollen Tube Localization Implies a Role in Pollen–Pistil Interactions for the Tomato Receptor-like Protein Kinases LePRK1 and LePRK2 , 1998, Plant Cell.

[156]  L. Cárdenas,et al.  Actin polymerization promotes the reversal of streaming in the apex of pollen tubes. , 2005, Cell motility and the cytoskeleton.

[157]  S. King The dynein microtubule motor. , 2000, Biochimica et biophysica acta.

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

[159]  K. Palme,et al.  Small GTPases in vesicle trafficking. , 2004, Current opinion in plant biology.

[160]  D. Yule,et al.  Phosphorylation of Inositol 1,4,5-Trisphosphate Receptors in Parotid Acinar Cells , 2002, The Journal of Biological Chemistry.

[161]  Zhenbiao Yang,et al.  ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. , 2003, Journal of experimental botany.

[162]  David Twell,et al.  AtCSLA7, a Cellulose Synthase-Like Putative Glycosyltransferase, Is Important for Pollen Tube Growth and Embryogenesis in Arabidopsis1 , 2003, Plant Physiology.