Skip to main content
SpringerLink
Log in

Development of male gametes in flowering plants

  • Minireview
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

The male gametes of angiosperms consist of two sperm cells within a pollen grain or a pollen tube. They are derived from a single generative cell, which is formed as the smaller cell by unequal cell division in the microspore after meiosis. Limited information is available about these male gametic cells, beyond observations by electron microscopy, because each is surrounded by the cytoplasm of a larger vegetative cell. Recently, large quantities of generative cells and sperm cells have been isolated from pollen grains or pollen tubes of various plant species, and their physiological, biochemical and molecular characterization is now possible. Although almost all the available results are still preliminary, it is evident that the male gametic cells are peculiar in terms both of cell structure and composition. For example, they are rich in axial microtubules which maintain the spindle-like shape of each cell. However, they lack plastids which are DNA-containing cytoplasmic organelles. Biochemical characterization of their proteins indicates the presence of male gamete-specific polypeptides. These findings suggest, not unexpectedly, the possibility of male gamete-specific gene expression and of a strict genetic mechanism that controls the formation of male gametes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Brown, R.C. andLemmon, B.E. 1991. Pollen development in orchids 3. A novel generative pole microtubule system predicts unequal pollen mitosis. J. Cell Sci.99: 273–281.

    Google Scholar 

  • Cass, D.D. 1973. An ultrastructural and Nomarski-interference study of the sperms of barley. Can. J. Bot.51: 601–605.

    Google Scholar 

  • Clauhs, R.P. andGrun, P. 1977. Changes in plastid and mitochondrial content during maturation of generative cells ofSolanum (Solanaceae). Amer. J. Bot.64: 377–383.

    Google Scholar 

  • Coleman, A.W. 1978. Visualization of chloroplast DNA with two fluorochromes. Exp. Cell Res.114: 95–100.

    Article  CAS  PubMed  Google Scholar 

  • Corriveau, J.L. andColeman, A.W. 1988. Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Amer. J. Bot.75: 1443–1458.

    Google Scholar 

  • Corriveau, J.L. andColeman, A.W. 1991. Monitoring by epifluorescence microscopy of organelle DNA fate during pollen development in five angiosperm species. Dev. Biol.147: 271–280.

    Article  CAS  PubMed  Google Scholar 

  • Cresti, M., Ciampolini, F. andKapil, R.N. 1984. Generative cells of some angiosperms with particular emphasis on their microtubules. J. Submicrosc. Cytol.16: 317–326.

    Google Scholar 

  • Cresti, M., Lancelle, S.A. andHepler, P.K. 1987. Structure of the generative cell wall complex after freeze substitution in pollen tubes ofNicotiana andImpatiens. J. Cell Sci.88: 373–378.

    Google Scholar 

  • Derksen, J., Pierson, E.S. andTraas, J.A. 1985. Microtubules in vegetative and generative cells of pollen tubes. Eur. J. Cell Biol.38: 142–148.

    Google Scholar 

  • Dickinson, H.G. 1990. Self-incompatibility in flowering plants. BioEssays12: 155–161.

    Article  Google Scholar 

  • Dumas, C., Knox, R.B. andGaude, T. 1985. The spatial association of the sperm cells and vegetative nucleus in the pollen grain ofBrassica. Protoplasma124: 168–174.

    Article  Google Scholar 

  • Erickson, R.P. 1990. Post-meiotic gene expression. Trends Genet.6: 264–269.

    CAS  PubMed  Google Scholar 

  • Geltz, N.R. andRussell, S.D. 1988. Two-dimensional electrophoretic studies of the proteins and polypeptides in mature pollen grains and the male germ unit ofPlumbago zeylanica. Plant Physiol.88: 764–769.

    CAS  Google Scholar 

  • Hagemann, R. andSchröder, M.B. 1989. The cytological basis of the plastid inheritance in angiosperms. Protoplasma152: 57–64.

    Article  Google Scholar 

  • Hanson, D.D., Hamilton, D.A., Travis, J.L., Bashe, D.M. andMascarenhas, J.P. 1989. Characterization of a pollen-specific cDNA clone fromZea mays and its expression. Plant Cell1: 173–179.

    CAS  PubMed  Google Scholar 

  • Haring, V., Gray, J.E., McClure, B.A., Anderson, M.A. andClarke, A.E. 1990. Self-incompatibility: a self-recognition system in plants. Science250: 937–941.

    CAS  PubMed  Google Scholar 

  • Haskell, D.W. andRogers, O.M. 1985. RNA synthesis by vegetative and sperm nuclei of trinucleate pollen. Cytologia50: 805–809.

    Google Scholar 

  • Heslop-Harrison, J. 1968. Synchronous pollen mitosis and the formation of the generative cell in massulate orchids. J. Cell Sci.3: 457–466.

    Google Scholar 

  • Heslop-Harrison, J. 1987. Pollen germination and pollen-tube growth. Int. Rev. Cytol.107: 1–78.

    Google Scholar 

  • Heslop-Harrison, J. andHeslop-Harrison, Y. 1989. Myosin associated with the surfaces of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes. J. Cell Sci.94: 319–325.

    Google Scholar 

  • Heslop-Harrison, J., Heslop-Harrison, Y., Cresti, M., Tiezzi, A. andMoscatelli, A. 1988. Cytoskeletal elements, cell shaping and movement in the angiosperm pollen tube. J. Cell Sci.91: 49–60.

    Google Scholar 

  • Hough, T., Singh, M.B., Smart, I.J. andKnox, R.B. 1986. Immunofluorescent screening of monoclonal antibodies to surface antigens of animal and plant cells bound to polycarbonate membranes. J. Immunol. Methods92: 103–107.

    Article  CAS  PubMed  Google Scholar 

  • James, T.W. andJope, C. 1978. Visualization by fluorescence of chloroplast DNA in higher plants by means of the DNA-specific probe 4′6-diamidino-2-phenylindole. J. Cell Biol.79: 623–630.

    Article  CAS  PubMed  Google Scholar 

  • Keller, W.A. andArmstrong, K.C. 1979. Stimulation of embryogenesis and haploid production inBrassica campestris anther cultures by elevated temperature treatments. Theor. Appl. Genet.55: 65–67.

    Article  Google Scholar 

  • Kohno, T., Chaen, S. andShimmen, T. 1990. Characterization of the translocator associated with pollen tube organelles. Protoplasma154: 179–183.

    Article  Google Scholar 

  • Kranz, E., Bautor, J. andLörz, H. 1991.In vitro fertilization of single, isolated gametes of maize mediated by electrofusion. Sex. Plant Reprod.4: 12–16.

    Google Scholar 

  • La Cour, LF. 1949. Nuclear differentiation in the pollen grain. Heredity3: 319–337.

    Google Scholar 

  • LaFountain, K.L. andMascarenhas, J.P. 1972. Isolation of vegetative and generative nuclei from pollen tubes. Exp. Cell Res.73: 233–236.

    Article  CAS  PubMed  Google Scholar 

  • Lee, C.H. andPower, J.B. 1988. Intraspecific gametosomatic hybridization inPetunia hybrida. Plant Cell Rep.7: 17–18.

    Google Scholar 

  • Maruyama, K., Gay, H. andKaufmann, B.P. 1965. The nature of the wall between generative and vegetative nuclei in the pollen grain ofTradescantia-paludosa. Amer. J. Bot.52: 605–610.

    CAS  Google Scholar 

  • Mascarenhas, J.P. 1975. The biochemistry of angiosperm pollen development. Bot. Rev.41: 259–314.

    CAS  Google Scholar 

  • Mascarenhas, J.P. 1989. The male gametophyte of flowering plants. Plant Cell1: 657–664.

    PubMed  Google Scholar 

  • Mascarenhas, J.P. 1990. Gene activity during pollen development. Annu. Rev. Plant Physiol. Plant Mol. Biol.41: 317–338.

    Article  Google Scholar 

  • Matthews, B.F., Abdul-Baki, A.A. andSaunders, J.A. 1990. Expression of a foreign gene in electroporated pollen grains of tobacco. Sex. Plant Reprod.3: 147–151.

    Article  Google Scholar 

  • McCormick, S. 1991. Molecular analysis of male gametogenesis in plants. Trends Genet.7: 298–303.

    CAS  PubMed  Google Scholar 

  • Miyamura, S., Kuroiwa, T. andNagata, T. 1987. Disappearance of plastid and mitochondrial nucleoids during the formation of generative cells of higher plants revealed by fluorescence microscopy. Protoplasma141: 149–159.

    Article  Google Scholar 

  • Nasrallah, J.B., Nishio, T. andNasrallah, M.E. 1991. The self-incompatibility genes ofBrassica: expression and use in genetic ablation of floral tissues. Annu. Rev. Plant Physiol. Plant Mol. Biol.42: 393–422.

    Article  Google Scholar 

  • Newton, K.J. 1988. Plant mitochondrial genomes: organization, expression and variation. Annu. Rev. Plant Physiol. Plant Mol. Biol.39: 503–532.

    Article  CAS  Google Scholar 

  • Palevitz, B.A. andCresti, M. 1988. Microtubule organization in the sperm ofTradescantia virginiana. Protoplasma146: 28–34.

    Article  Google Scholar 

  • Pennell, R.I., Geltz, N.R., Koren, E. andRussell, S.D. 1987. Production and partial characterization of hybridoma antibodies elicited to the sperm ofPlumbago zeylanica. Bot. Gaz.148: 401–406.

    Article  Google Scholar 

  • Pipkin, J.L. andLarson, D.A. 1973. Changing patterns of nucleic acids, basic and acidic proteins in generative and vegetative nuclei during pollen germination and pollen tube growth inHippeastrum belladonna. Exp. Cell Res.79: 28–42.

    CAS  PubMed  Google Scholar 

  • Pirrie, A. andPower, J.B. 1986. The production of fertile, triploid somatic hybrid plants (Nicotiana glutinosa (n)+N. tabacum (2n)) via gametic: somatic protoplast fusion. Theor. Appl. Genet.72: 45–52.

    Article  Google Scholar 

  • Raghavan, V. 1987. Developmental strategies of the angiosperm pollen: a biochemical perspective. Cell Differ.21: 213–226.

    Article  CAS  PubMed  Google Scholar 

  • Reynolds, T.L. andRaghavan, V. 1982. An autoradiographic study of RNA synthesis during maturation and germination of pollen grains ofHyoscyamus niger. Protoplasma111: 177–188.

    Article  CAS  Google Scholar 

  • Riggs, C.D. andHasenkampf, C.A. 1991. Antibodies directed against a meiosis-specific, chromatin-associated protein identify conserved meiotic epitopes. Chromosoma101: 92–98.

    Article  CAS  PubMed  Google Scholar 

  • Russell, S.D. 1985. Preferential fertilization inPlumbago: ultrastructural evidence for gamete-level recognition in an angiosperm. Proc. Natl. Acad. Sci.82: 6129–6132.

    CAS  Google Scholar 

  • Russell, S.D. 1986. Isolation of sperm cells from the pollen ofPlumbago zeylanica. Plant Physiol. 81: 317–319.

    Google Scholar 

  • Russell, S.D. 1991. Isolation and characterization of sperm cells in flowering plants. Annu. Rev. Plant Physiol. Plant Mol. Biol.42: 189–204.

    Article  CAS  Google Scholar 

  • Russell, S.D., Cresti, M. andDumas, C. 1990. Recent progress on sperm characterization in flowering plants. Physiol. Plant.80: 669–676.

    Article  Google Scholar 

  • Sanger, J.M. andJackson, W.T. 1971a. Fine structure study of pollen development inHaemanthus katherinae Baker I. Formation of vegetative and generative cells. J. Cell Sci.8: 289–301.

    CAS  PubMed  Google Scholar 

  • Sanger, J.M. andJackson, W.T. 1971b. Fine structure study of pollen development inHaemanthus katherinae Baker II. Microtubules and elongation of the generative cells. J. Cell Sci.8: 303–315.

    CAS  PubMed  Google Scholar 

  • Sasaki, Y., Yasuda, H., Ohba, Y. andHarada, H. 1990. Isolation and characterization of a novel nuclear protein from pollen mother cells of lily. Plant Physiol.94: 1467–1471.

    CAS  Google Scholar 

  • Sax, K. 1935. The effects of temperature on nuclear differentiation in microspore development. J. Arnold Arboretum.16: 301–310.

    Google Scholar 

  • Scott, R., Hodge, R., Paul, W. andDraper, J. 1991. The molecular biology of anther differentiation. Plant Sci.80: 167–191.

    Article  CAS  Google Scholar 

  • Shivanna, K.R., Xu, H., Taylor, P. andKnox, R.B. 1988. Isolation of sperms from the pollen tubes of flowering plants during fertilization. Plant Physiol.87: 647–650.

    Google Scholar 

  • Stanley, R.G. andLinskens, H.F. 1974. Pollen. Springer-Verlag, Berlin.

    Google Scholar 

  • Sunderland, N. andWicks, F.M. 1971. Embryoid formation in pollen grains ofNicotiana tabacum. J. Exp. Bot.22: 213–226.

    Google Scholar 

  • Tanaka, I. 1988. Isolation of generative cells and their protoplasts from pollen ofLilium longiflorum. Protoplasma142: 68–73.

    Article  Google Scholar 

  • Tanaka, I. 1991. Microtubule-determined plastid distribution during microsporogenesis inLilium longiflorum. J. Cell Sci.99: 21–31.

    CAS  Google Scholar 

  • Tanaka, I. andIto, M. 1981a. Studies on microspore development in liliaceous plants III. Pollen tube development in lily pollens cultured from the uninucleate microspore stage. Plant Cell Physiol.22: 149–153.

    Google Scholar 

  • Tanaka, I. andIto, M. 1981b. Control of division patterns in explanted microspores ofTulipa gesneriana. Protoplasma108: 329–340.

    Article  Google Scholar 

  • Tanaka, I., Kitazume, C. andIto, M. 1987. The isolation and culture of lily pollen protoplasts. Plant Sci.50: 205–211.

    Article  CAS  Google Scholar 

  • Tanaka, I., Nakamura, S. andMiki-Hirosige, H. 1989. Structural features of isolated generative cells and their protoplasts from pollen of some liliaceous plants. Gamete Res.24: 361–374.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, J.H. andMcMaster, R.D. 1954. Autoradiographic and microphotometric studies of deoxyribose nucleic acid during microgametogenesis inLilium longiflorum. Chromosoma6: 489–521.

    CAS  PubMed  Google Scholar 

  • Taylor, P., Kenrick, J., Li, Y., Kaul, V., Gunning, B.E.S. andKnox, R.B. 1989. The male germ unit ofRhododendron: quantitative cytology, three-dimensional reconstruction, isolation and detection using fluorescent probes. Sex. Plant Reprod.2: 254–264.

    Article  Google Scholar 

  • Terasaka, O. andNiitsu, T. 1990. Unequal cell division and chromatin differentiation in pollen grain cells II. Microtubule dynamics associated with the unequal cell division. Bot. Mag. Tokyo103: 133–142.

    Google Scholar 

  • Theunis, C.H., Pierson, E.S. andCresti, M. 1991. Isolation of male and female gametes in higher plants. Sex. Plant Reprod.4: 145–154.

    Article  Google Scholar 

  • Theunis, C.H., Pierson, E.S. andCresti, M. 1992. The microtubule cytoskeleton and the rounding of isolated generative cells ofNicotiana tabacum. Sex. Plant Reprod.5: 64–71.

    Article  Google Scholar 

  • Thiébaud, C.H. andRuch, F. 1978. Cytophotometric study of nuclear differentiation during pollen development inTradescantia paludosa. Histochem.57: 119–128.

    Article  Google Scholar 

  • Twell, D., Klein, T.M., Fromm, M.E. andMcCormick, S. 1989a. Transient expression of chimeric genes delivered into pollen by microprojectile bombardment. Plant Physiol.91: 1270–1274.

    CAS  Google Scholar 

  • Twell, D., Wing, R., Yamaguchi, J. andMcCormick, S. 1989b. Isolation and expression of an anther-specific gene from tomato. Mol. Gen. Genet.217: 240–245.

    CAS  PubMed  Google Scholar 

  • Ueda, K., Miyamoto, Y. andTanaka, I. 1990. Fusion studies of pollen protoplasts and generative cell protoplasts inLilium longiflorum. Plant Sci.72: 259–266.

    Article  Google Scholar 

  • Wagner, V.T., Dumas, C. andMogensen, H.L. 1989. Morphometric analysis of isolatedZea mays sperm. J. Cell Sci.93: 179–184.

    Google Scholar 

  • Wenzel, G., Hoffman, F. andThomas, E. 1977. Increased induction and chromosome doubling of androgenetic haploid rye. Theor. Appl. Genet.51: 81–86.

    Article  Google Scholar 

  • Zaki, M.A.M. andDickinson, H.G. 1991. Microspore-derived embryos inBrassica: the significance of division symmetry in pollen mitosis I to embryogenic development. Sex. Plant Reprod.4: 48–55.

    Article  Google Scholar 

  • Zhou, C., Zee, S.Y. andYang, H.Y. 1990. Microtubule organization of in situ and isolated generative cells inZephyranthes grandiflora Lindl. Sex. Plant Reprod.3: 213–218.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Yokohama City University, Seto 22-2, Kanazawa-ku, 236, Yokohama, Japan

    Ichiro Tanaka

Authors
  1. Ichiro Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tanaka, I. Development of male gametes in flowering plants. J. Plant Res. 106, 55–63 (1993). https://doi.org/10.1007/BF02344373

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02344373

Key words

Search

Navigation