Abstract
The growth of pollen tubes is characterized by an intense cytoplasmic streaming, during which the movements of smaller organelles (like secretory vesicles) and larger ones (including the generative cell and vegetative nucleus) are precisely coordinated. A well-characterized cytoskeletal apparatus is likely responsible for these intracellular movements. In recent years both microfilament and microtubule-based motor proteins have been identified and assumed to be the translocators of the several organelle categories. Their precise function during pollen tube growth is not yet clear, but apparently an actomyosin-based system is mainly responsible for pollen tube elongation. On the other hand, microtubules and microtubule-based motors have been thought to play a role in the maintenance of cell polarity. Both cytoskeletal systems (and their respective motor activities) could cooperate to ensure a precise regulation of pollen tube growth.
Similar content being viewed by others
References
Asada T, Shibaoka H (1994) Isolation of polypeptides with microtubule-translocating activity from phragmoplasts of tobacco BY-2 cells. J Cell Sci 107:2249–2257
Asada T, Seonobe S, Shibaoka H (1991) Microtubule translocation in the cytokinetic apparatus of cultured tobacco cells. Nature 350:238–241
Åström H, Sorri O, Raudaskoski M (1995) Role of microtubules in the movement of the vegetative nucleus and generative cell in tobacco pollen tubes. Sex Plant Reprod 8:61–69
Cai G, Bartalesi A, Del Casino C, Moscatelli A, Tiezzi A, Cresti M (1993) The kinesin-immunoreactive homologue fromNicotiana tabacum pollen tube: biochemical properties and subcellular localization. Planta 191:496–506
Cai G, Moscatelli A, Del Casino C, Chevrier V, Mazzi M, Tiezzi A, Cresti M (1996) The anti-centrosome mAb 6C6 reacts with a plasma membrane-associated polypeptide of 77-kDa from theNicotiana tabacum pollen tubes. Protoplasma 190:68–78
Cohn SA (1990) The mechanochemistry of kinesin. Mol Chem Neuropathol 12:83–94
Cyr RJ, Palevitz BA (1995) Organization of cortical microtubules in plant cells. Curr Opin Cell Biol 7:65–71
Del Casino C, Li YQ, Moscatelli A, Scali M, Tiezzi A, Cresti M (1993) Distribution of microtubules during the growth of tobacco pollen tubes. Biol Cell 79:125–132
Derksen J, Pierson ES, Traas JA (1985) Microtubules in vegetative and generative cells of pollen tubes. Eur J Cell Biol 38:142–148
Derksen J, Rutten T, Amstel T van, Win A de, Doris F, Steer M (1995) Regulation of pollen tube growth. Acta Bot Neerl 44:93–119
Dillman JF, Pfister KK (1994) Differential phosphorylation in vivo of cytoplasmic dynein associated with anterogradely moving organelles. J Cell Biol 127:1671–1681
Eshel D, Urrestarazu LA, Vissers S, Jauniaux JC, Vliet-Reedijk JC van, Planta RJ, Gibbons IR (1993) Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc Natl Acad Sci USA 90:11172–11176
Fath KR, Trimbur GM, Burgess DR (1994) Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J Cell Biol 126:661–675
Franke WW, Herth W, VanDerWoude W, Morré DJ (1972) Tubular and filamentous structures in pollen tubes: possible involvement as guide elements in protoplasmic streaming and vectorial migration of secretory vesicles. Planta 105:217–341
Hepler PK, Palevitz BA, Lancelle SA, McCauley MM, Lichtscheidl I (1990) Cortical endoplasmic reticulum in plants. J Cell Sci 96:355–373
Heslop-Harrison J, Heslop-Harrison Y (1989a) Myosin associated with the surface of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes. J Cell Sci 94:319–325
Heslop-Harrison J, Heslop-Harrison Y (1989b) Actomyosin and movement in the angiosperm pollen tube: an interpretation of some recent results. Sex Plant Reprod 2:199–207
Heslop-Harrison J, Heslop-Harrison Y, Cresti M, Tiezzi A, Moscatelli A (1988) Cytoskeletal elements, cell shaping and movement in the angiosperm pollen tube. J Cell Sci 91:49–60
Hirokawa N, Sato-Yoshitake R, Yoshida T, Kawashima T (1990) Brain dynein (MAPIC) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J Cell Biol 111:1027–1037
Hirokawa N, Sato-Yoshitake R, Kobayashi N, Pfister KK, Bloom GS, Brady ST (1991) Kinesin associates with anterogradely transported membranous organelles in vivo. J Cell Biol 114:295–302
Houliston E, Elinson RP (1991) Evidence for the involvement of microtubules, ER, and kinesin in the cortical rotation of fertilized frog eggs. J Cell Biol 114:1017–1028
Hush JM, Wadsworth P, Callaham DA, Hepler PK (1994) Quantitation of microtubule dynamics in living plant cells using fluorescence redistribution after photobleaching. J Cell Sci 107:775–784
Joos U, Aken J van, Kristen U (1994) Microtubules are involved in maintaining the cellular polarity in pollen tubes ofNicotiana sylvestris. Protoplasma 179:5–15
Joos U, Aken J van, Kristen U (1995) The anti-microtubule drug carbetamide stopsNicotiana sylvestris pollen tube growth in the style. Protoplasma 187:182–191
Khono T, Shimmen T (1988) Accelerated sliding of pollen tube organelles along Characeae actin bundles regulated by Ca2+. J Cell Biol 106:1539–1543
Khono T, Chaen S, Shimmen T (1990) Characterization of the translocator associated with pollen tube organelles. Protoplasma 154:179–183
Khono T, Ishikawa R, Nagata T, Kohama K, Shimmen T (1992) Partial purification of myosin from lily pollen tubes by monitoring with in vitro motility assay. Protoplasma 170:77–85
Lancelle SA, Hepler PK (1991) Association of actin with cortical microtubules revealed by immunogold localization inNicotiana pollen tubes. Protoplasma 165:167–172
Langford GM (1995) Actin- and microtubule-dependent organelle motors: interrelationships between the two motility system. Curr Opin Cell Biol 7:82–88
Lillie SH, Brown SS (1992) Suppression of a myosin defect by a kinesin-related gene. Nature (London) 356:358–361
Liu GQ, Cai G, Del Casino C, Tiezzi A, Cresti M (1994) Kinesin-related polypeptide is associated with vesicles fromCorylus avellana pollen. Cell Motil Cytoskeleton 29:155–166
Mascarenhas JP (1993) Molecular mechanisms of pollen tube growth and differentiation. Plant Cell 5:1303–1314
Matthies HJG, Miller RJ, Palfrey HC (1993) Calmodulin binding to and CAMP-dependent phosphorylation of kinesin light chains modulate kinesin ATPase activity. J Biol Chem 268:11176–11187
Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes ofLilium. J Cell Sci 101:7–12
Miller DD, Scordilis SP, Hepler PK (1995) Identification and localization of three classes of myosins in pollen tubes ofLilium longiflorum andNicotiana alata. J Cell Sci 108:2549–2563
Mitsui H, Nakatani K, Yamaguchi-Shinozaki K, Shinozaki K, Nishikawa K, Takahashi H (1994) Sequencing and characterization of the kinesin-related geneskatB andkatC ofArabidopsis thaliana. Plant Mol Biol 25:865–876
Miyake T, Kuroiwa H, Kuroiwa T (1995) Differential mechanisms of movement between a generative cell and a vegetative nucleus in pollen tubes ofNicotiana tabacum as revealed by additions of colchicine and nonanoic acid. Sex Plant Reprod 8:228–230
Moscatelli A, Del Casino C, Lozzi L, Cai G, Scali M, Tiezzi A, Cresti M (1995) High molecular weight polypeptides related to dynein heavy chains inNicotiana tabacum pollen tubes. J Cell Sci 108:1117–1125
Okagaki T, Ishikawa R, Kohama K (1991) Inhibitory Ca2+-regulation of myosin light chain kinase in the lower eucaryote,Physarum polycephalum: role of a Ca2+ dependent inhibitory factor. Eur J Cell Biol 56:113–122
Palevitz BA, Liu B, Joshi C (1994) γ-tubulin in tobacco pollen tubes: association with generative cell and vegetative microtubules. Sex Plant Reprod 7:209–214
Pierson ES, Cresti M (1992) Cytoskeleton and cytoplasmic organization of pollen and pollen tubes. Int Rev Cytol 140:73–125
Pierson ES, Derksen J, Traas JA (1986) Organization of microfilaments and microtubules in pollen tubes grown in vitro or in vivo in various angiosperms. Eur J Cell Biol 41:14–18
Pierson ES, Lichtscheidl IK, Derksen J (1990) Structure and behaviour of organelles in living pollen tubes ofLilium longiflorum. J Exp Bot 41:1461–1468
Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, Cresti M, Hepler PK (1994) Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell 6:1815–1828
Sato-Yoshitake R, Shiomura Y, Myyasaka H, Hirokawa N (1992) The phosphorylation of kinesin regulates its binding to synaptic vesicles. J Biol Chem 267:23930–23936
Saunders WS, Koshland D, Eshel D, Gibbons IR, Hoyt MA (1995)Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J Cell Biol 128:617–624
Scali M, Cai G, Del Casino C, Santucci A, Tirlapur UK, Moscatelli A, Cresti M, Tiezzi A (1994) Purification and biochemical characterization of calmodulin fromCorylus avellana pollen. Plant Physiol Biochem 32:831–838
Tang X, Hepler PK, Scordilis SP (1989) Immunochemical and immunocytochemical identification of a myosin heavy chain polypeptide inNicotiana pollen tube. J Cell Sci 92:569–574
Terasaka O, Niitsu T (1994) Differential roles of microtubule and actin-myosin cytoskeleton in the growth ofPinus pollen tubes. Sex Plant Reprod 7:264–272
Tiezzi A, Moscatelli A, Cai G, Bartalesi A, Cresti M (1992) An immunoreactive homolog of mammalian kinesin inNicotiana tabacum pollen tubes. Cell Motil Cytoskeleton 21:132–137
Tirlapur UK, Scali M, Moscatelli A, Del Casino C, Cai G, Tiezzi A, Cresti M (1994) Confocal image analysis of spatial variations in immunocytochemically identified calmodulin during pollen hydration, germination and pollen tube tip growth inNicotiana tabacum L. Zygote 2:63–68
Tirlapur U, Cai G, Faleri C, Moscatelli A, Scali M, Del Casino C, Tiezzi A, Cresti M (1995) Confocal imaging and immunogold electron microscopy of changes in distribution of myosin during pollen hydration, germination and pollen tube growth inNicotiana tabacum L. Eur J Cell Biol 67:209–217
Tirlapur UK, Faleri C, Cresti M (1996) Immunoelectron microscopy of myosin associated with the generative cells in pollen tubes ofNicotiana tabacum L. Sex Plant Reprod (in press)
Tiwari SC, Polito VS (1988) Organization of the cytoskeleton in pollen tubes ofPyrus communis: a study employing conventional and freeze-substituted electron microscopy, immunofluorescence, and rhodamine-phalloidin. Protoplasma 147:100–112
Tiwari SC, Polito VS (1990) The initiation and organization of microtubules in germinating pear (Pyrus communis L.) pollen. Eur J Cell Biol 53:384–389
Vaisberg EA, Koonce MP, McIntosh JR (1993) Cytoplasmic dynein plays a role in mammalian mitotic spindle formation. J Cell Biol 123:849–858
Yang C, Xing L, Zhai Z (1992) Intermediate filaments in higher plant cells and their assembly in a cell-free system. Protoplasma 171:44–54
Yokota E, Shimmen T (1994) Isolation and characterization of plant myosin from pollen tubes of lily. Protoplasma 177:153–162
Yokota E, McDonald AR, Liu B, Shimmen T, Palevitz BA (1995) Localization of a 170 kDa myosin heavy chain in plant cells. Protoplasma 185:178–187
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cai, G., Moscatelli, A., Del Casino, C. et al. Cytoplasmic motors and pollen tube growth. Sexual Plant Reprod 9, 59–64 (1996). https://doi.org/10.1007/BF02153052
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02153052