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Cytoskeletal organisation and modification during pollen tube arrival, gamete delivery and fertilisation in Plumbago zeylanica

Published online by Cambridge University Press:  26 September 2008

Bing-Quan Huang ,
Elisabeth S. Pierson ,
Scott D. Russell ,
Antonio Tiezzi  and
Mauro Cresti
Bing-Quan Huang
Affiliation:
University of Oklahoma, USA, and University of Siena, Italy.
Elisabeth S. Pierson
Affiliation:
University of Oklahoma, USA, and University of Siena, Italy.
Scott D. Russell*
Affiliation:
University of Oklahoma, USA, and University of Siena, Italy.
Antonio Tiezzi
Affiliation:
University of Oklahoma, USA, and University of Siena, Italy.
Mauro Cresti
Affiliation:
University of Oklahoma, USA, and University of Siena, Italy.
*
*Scott D.Russell, Department of Botany and Microbilolgy, University of Oklahoma, Norman, OK 73019-0245, USA.
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Extract

The cytoskeletal organisation of the isolated embryo sac and egg cells of Plumbago zeylanica was examined before, during and after pollen tube penetration into the embryo sac to determine the potential involvement of microtubules and actin filaments in fertilisation. Material was singly and triply stained using Hoechst 33258 to localise DNA, fluorescein isothiocyanate (FITC)-labelled anti- α-tubulin to detect microtubules and rhodamine-phalloidin to visualise F-actin. Microtubules in the unfertilised egg cell are longitudinally aligned in the micropylar and mid-lateral areas, aggregating into bundles near the filiform apparatus. In the perinuclear cytoplasm of the egg cell, microtubules become more or less randomly aligned. F-actin bundles form a longitudinally aligned mesh in the chalazal cytoplasm of the egg cell. In the central cell, microtubules and F-actin are distributed along transvacuolar strands and are also evident in the perinuclear region and at the periphery of the cell. During pollen tube penetration, sparse microtubule bundles near the pathway of the pollen tube may form an apparent microtubular ‘conduit’ surrounding the male gametes at the delivery site. Actin aggregates become organised near the pathway of the pollen tube and at the delivery site of the sperm cells. Subsequently, actin aggregates form a ‘corona’ structure in the intercellular region between the egg and central cell where gametic fusion occurs. The corona may have a role in maintaining the close proximity of the egg and central cell and helping the two sperm cells move and bind to their target cells. The cytoskeleton may also be involved in causing the two nuclei of the egg and central cell to approach one another at the site of gametic fusion and transporting the two sperm nuclei into alignment with their respective female nucleus. The cytoskeleton is reorganised during early embryogenesis.

Keywords

ActinCytoskeletonFertilisationGamete FusionMicrotubulesPlumbago
Type
Article
Information
Zygote , Volume 1 , Issue 2 , May 1993 , pp. 143 - 154
Copyright
Copyright © Cambridge University Press 1993

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References

Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., Watson, J.D. (1989). Molecular biology of the cell, 2nd edn. New York: Garland Publishing.Google Scholar
Bednara, J., van Lammeren, A.A.M., Willemse, M.T.M. (1988). Microtubular configurations during meiosis and megasporogenesis in Gasteria verrucosa and Chamaenerion angustifolium. Sex. Plant Reprod. 1, 164–72.CrossRefGoogle Scholar
Bednara, J., Willemse, M.T.M., van Lammeren, A.A.M. (1990). Organisation of the actin cytoskeleton during megasporogenesis in Gasteria verrucosa visualized with fluorescent-labelled phalloidin. Acta Bot. Neerl. 39, 43–8.CrossRefGoogle Scholar
Cass, D.D. (1972). Occurrence and development of a filiform apparatus in the egg of Plumbago capensis. Am. J. Bot. 59, 279–83.Google Scholar
Cass, D.D., Karas, I. (1974). Ultrastructural organisation of the egg of Plumbago zeylanica. Protoplasma 81, 49–62.CrossRefGoogle ScholarPubMed
Emons, A.M., Pierson, E.S., Derksen, J. (1991). Cytoskeleton and intracellular movement in plant cells. In Biotechnology: Current Progress, eds. Cheremisinoff, P.N. and Ferrante, L., pp. 311–35. Basel: Technomic Publ.Google Scholar
Erdelská, O. (1974). Contribution to the study of fertilization in the living embryo sac. In Fertilization in Higher Plants, ed. Linskens, H.F., pp. 191–5. Amsterdam: North-Holland.Google Scholar
Erdelská, O. (1983). Microcinematographical investigation of the female gametophyte, fertilisation and early embryo and endosperm development. In Fertilization and Embryogenesis in Ovulated Plants, ed. Erdelsk´, O., pp. 49–54. Bratislava, Czechoslovakia: VEDA.Google Scholar
Heslop-Harrison, J., Heslop-Harrison, Y. (1989a). Actomyosin and movement in the angiosperm pollen tube. Sex. Plant Reprod. 3, 187–94.Google Scholar
Heslop-Harrison, J., Heslop-Harrison, Y. (1989b). Myosin associated with the surfaces of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes. J. Cell Sci. 94, 319–25.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Huang, B.Q. & Russell, S.D. (1989). Isolation of fixed and viable eggs, central cells and embryo sacs from ovules of Plumbago zeylanica. Plant Physiol. 90, 9–12.CrossRefGoogle ScholarPubMed
Huang, B.Q. & Russell, S.D. (1992a). Female germ unit: organisation, isolation and function. Int. Rev. Cytol. 140, 133–93.Google Scholar
Huang, B.Q. & Russell, S.D. (1992b). The ultrastructural organisation of freeze-substituted ovules of Nicotiana tabacum before and after fertilisation. XII International Congress on Sexual Plant Reproduction (abstract), pp. 29–30.Google Scholar
Huang, B.Q., Russell, S.D., Strout, G.W., Mao, L.J. (1990). Organisation of isolated embryo sacs and eggs of Plumbago zeylanica (Plumbaginaceae) before and after fertilisation. Amer. J. Bot. 77, 1401–10.Google Scholar
Huang, B.Q., Pierson, E.S., Russell, S.D., Tiezzi, A., Cresti, M.(1992). Video microscopic observations of living, isolated embryo sacs of Nicotiana and their component cells. Sex. Plant Reprod. 5, 156–62.Google Scholar
Kohno, T., Chaen, S., Shimmen, T. (1990). Characterisation of the translocator associated with pollen tube organelles. Protoplasma 154, 179–83.CrossRefGoogle Scholar
Kuroda, K. (1989). Cytoplasmic streaming in plant cells. Int. Rev. Cytol. 121, 267–307.Google Scholar
Lancelle, SA, Hepler, P.K. (1991) Association of actin with cortical microtubules revealed by immunogold localisation in Nicotiana pollen grains. Protoplasma 165: 167–72CrossRefGoogle Scholar
Lancelle, S.A., Cresti, M., Hepler, P.K. (1987). Ultrastructure of the cytoskeleton in the freeze-substituted pollen tubes of Nicotiana alata. Protoplasma 140, 141–50.CrossRefGoogle Scholar
Palevitz, B.A., Tiezzi, A. (1992). Organization, composition and function of the generative cell and sperm cytoskeleton. Int. Rev. Cytol. 140, 149–86.CrossRefGoogle Scholar
Pierson, E.S., Cresti, M. (1992). Cytoskeleton and cytoplasmic organisation of pollen and pollen tubes. Int. Rev. Cytol. 140, 73–128.CrossRefGoogle Scholar
Pierson, E.S., Kengen, H.M.P., Derksen, J. (1989). Microtubules and actin filaments co-localise in pollen tubes of Nicotiana tabacum L.and Lilium longiflorum Thunb. Protoplasma 150, 75–7.CrossRefGoogle Scholar
Russell, S.D. (1982). Fertilisation in Plumbago zeylanica: entry and discharge of the pollen tube into the embryo sac. Can. J. Bot. 60, 2219–30.CrossRefGoogle Scholar
Russell, S.D. (1983). Fertilisation in Plumbago zeylanica: gametic fusion and fate of the male cytoplasm. Am. J. Bot. 70, 416–34.CrossRefGoogle Scholar
Russell, S.D. (1984). Ultrastructure of the sperm of Plumbago zeylanica. II. Quantitative cytology and three-dimensional reconstruction. Planta 162, 385–91.CrossRefGoogle Scholar
Russell, S.D. (1985). Preferential fertilisation in Plumbago:ultrastructural evidence for gamete-level recognition in an angiosperm. Proc. Natl. Acad. Sci. USA 82, 6129–32.CrossRefGoogle Scholar
Russell, S.D. (1989). Preferential fertilisation in the synergid-lacking angiosperm Plumbago zeylanica. Phytomorphology 39, 1–20.Google Scholar
Russell, S.D. (1992). Double fertilization. Int. Rev. Cytol. 140, 357–88.CrossRefGoogle Scholar
Russell, S.D., Huang, B.Q. (1992). Cytoskeletal organisation within the embryo sac before and after fertilisation in Nicotiana and Plumbago. XII International Congress on Sexual Plant Reproduction (abstract), p. 58.Google Scholar
Russell, S.D., Huang, B.Q., Strout, G.W. (1989). Preliminary intermediate voltage electron microscopic observations of the isolated embryos sacs and eggs of Plumbago zeylanica L. (Plumbaginaceae). In Some Aspects and Actual Orientations in Plant Embryology, pp. 109–19. Université de Picardie, Faculté des Sciences.Google Scholar
Staiger, C.J. & Schliwa, M. (1987). Actin localisation and function in higher plants. Protoplasma 141, 1–12.Google Scholar
Tang, X., Hepler, P.K., Scordilis, S.P. (1989). Immunochemical and immunocytochemical identification of a myosin heavy chain polypeptide in Nicotiana pollen tubes. J. Cell. Sci. 92, 569–74.CrossRefGoogle ScholarPubMed
Webb, M.C., Gunning, B.E.S. (1990). Embryo sac development in Arabidopsis thaliana. I. Megasporogenesis, including the microtubular cytoskeleton. Sex. Plant Reprod. 3, 244–56.CrossRefGoogle Scholar
Webb, M.C., Gunning, B.E.S. (1991). The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184, 187–95.CrossRefGoogle ScholarPubMed
Willemse, M.T.M., & van Lammeren, A.A.M. (1988). Structure and function of the microtubular cytoskeleton during megasporogenesis and embryo sac development in Gasteria verrucosa (Mill.) H. Duval. Sex. Plant Reprod. 1, 74–82.Google Scholar