Contribution to the Knowledge of Fertilization of Gymnosperms with Flagellated Sperm Cells: Ginkgo biloba and Cycas revoluta

  • Terumitsu Hori
  • Shin-ichi Miyamura


It was Strasburger [1] who first drew attention to fertilization in Ginkgo biloba. He followed the development of the embryonic sac and embryo as well as the formation of the female gametophyte. Much later, as a result of his study on fertilization in Juniperus virginiana, he argued in favor of the existence of canal cells in Ginkgo and contributed to the knowledge of the development of the embryo [2]; however, he did not make any observations on fertilization himself. His last work on Ginkgo was on the development of the pollen [3].


Pollen Tube Sperm Cell Male Gametophyte Spermatogenous Cell Sperm Nucleus 
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  1. 1.
    Strasburger E (1872) Die Coniferen und die Gnetaceen. JenaGoogle Scholar
  2. 2.
    Strasburger E (1878) Über Befruchtung und Zellteilung. JenaGoogle Scholar
  3. 3.
    Strasburger E (1892) Über das Verhalten des Pollens und die Befruchtungs Vorgänge bei den Gymnospermen. Histol Beitr 4, JenaGoogle Scholar
  4. 4.
    Hirase S (1894) On the fecundation of Ginkgo biloba (in Japanese). Bot Mag Tokyo 8: 7–9Google Scholar
  5. 5.
    Hirase S (1895) Études sur le fécondation et l’embryogénie du Ginkgo biloba (1). J Coll Sc Imp Univ Tokio 8: 307–322Google Scholar
  6. 6.
    Hirase S (1894) Notes on the attraction-spheres in the pollen-cells of Ginkgo biloba. Bot Mag Tokyo 8: 359–360Google Scholar
  7. 7.
    Hirase S (1896a) Spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 10: 171–172Google Scholar
  8. 8.
    Hirase S (1896b) Observation on the behavior of the spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 10: 366Google Scholar
  9. 9.
    Hirase S (1896c) On the spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 10: 325–328Google Scholar
  10. 10.
    Hirase S (1897) Untersuchungen über das Verhalten des Pollens von Ginkgo biloba. Bot Centbl 69: 33–35Google Scholar
  11. 11.
    Ikeno S, Hirase S (1897) Spermatozoids in gymnosperms. Ann Bot 11: 344–345Google Scholar
  12. 12.
    Hirase S (1898) Études sur la fécondation et l’embryogenie du Ginkgo biloba (second mémoire). J Coli Sc Univ Imp Tokyo 12: 103–149Google Scholar
  13. 13.
    Webber HJ (1897b) Notes on the fecundation of Zamia and the pollen tube apparatus of Ginkgo. Bot Gaz 24: 225–235CrossRefGoogle Scholar
  14. 14.
    Fujii K (1898) Has the spermatozoid of Ginkgo a tail or none? (in Japanese). Bot Mag Tokyo 12: 287–290Google Scholar
  15. 15.
    Fujii K (1899a) Observations on the morphology of the pollen tube and the spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 13: 28–30Google Scholar
  16. 16.
    Fujii K (1899b) Remarks on Mr. Ikeno’s remarks on my views regarding the morphology of the pollen-cells and the spermatozoid of Ginkgo (in Japanese). Bot Mag Tokyo 13: 65–73Google Scholar
  17. 17.
    Fujii K (1899c) On the morphology of the spermatozoid of Ginkgo biloba (Preliminary note) (in Japanese). Bot Mag Tokyo 13: 260–266Google Scholar
  18. 18.
    Fujii K (1900) On the bicephalous spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 14: 16–17Google Scholar
  19. 19.
    Miyake K (1898) On the spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 12: 333–339Google Scholar
  20. 20.
    Miyake K (1902) The spermatozoid of Ginkgo. Notes on the morphology and methods. J Appi Micro Lab Metho 5: 1773–1780Google Scholar
  21. 21.
    Ikeno S (1899a) On the spermatozoid and pollen tube of Ginkgo biloba and Cycas revoluta (in Japanese). Bot Mag Tokyo 13: 31–34Google Scholar
  22. 22.
    Ikeno S (1899b) Opinion of various authors on the centrosome in the pollen tube of Cycadaceae and Ginkgo biloba (in Japanese). Bot Mag Tokyo 13: 74–76Google Scholar
  23. 23.
    Ikeno S (1928) Spermatozoids of Ginkgo biloba and Cycas revoluta (in Japanese). Shizenkagaku 3: 14–28Google Scholar
  24. 24.
    Bessey EA (1901) Notes on the spermatozoids of Ginkgo. Science 13: 255Google Scholar
  25. 25.
    Herzfeld S (1927) Beiträge zur Kenntnis von Ginkgo. Jahrb wiss Bot 66: 814–862Google Scholar
  26. 26.
    Shimamura T (1937) On the spermatozoid of Ginkgo biloba. Cytologia (Fujii Jubi Vol): 416–423Google Scholar
  27. 27.
    Lee CL (1955) Fertilization in Ginkgo biloba. Bot Gaz 117: 79–100CrossRefGoogle Scholar
  28. 28.
    Favre-Duchartre M (1956) Contribution à l’étude de la reproduction chez le Ginkgo biloba. Rev Cytol Biol Veg 17: 1–218Google Scholar
  29. 29.
    Tulecke WR (1957) The pollen of Ginkgo biloba: in vitro culture and tissue formation. Amer J Bot 44: 602–608CrossRefGoogle Scholar
  30. 30.
    Gifford EM, Lin J (1975) Light microscope and ultrastructural studies on the male gametophyte in Ginkgo biloba: the spermatogenous cell. Amer J Bot 62: 974–981CrossRefGoogle Scholar
  31. 31.
    Gifford EM, Larson S (1980) Developmental features of the spermatogenous cell in Ginkgo biloba. Amer J Bot 67: 119–124CrossRefGoogle Scholar
  32. 32.
    Rohr R (1980) Dévelopment in vitro du pollen de Ginkgo biloba L. Cytologia 45: 481–95CrossRefGoogle Scholar
  33. 33.
    Friedman WF (1987a) Growth and développement of the male gametophyte of Ginkgo biloba within the ovule (in vivo). Amer J Bot 74: 1797–1815CrossRefGoogle Scholar
  34. 34.
    Friedman WF (1987b) Morphogenesis and experimental aspects of growth and development of the male gametophyte of Ginkgo biloba in vitro. Amer J Bot 74: 1816–1830CrossRefGoogle Scholar
  35. 35.
    Friedman WF, Gifford EM (1987) Division of the generative cell and late development in the male gametophyte of Ginkgo biloba. Amer J Bot 75: 1434–1442CrossRefGoogle Scholar
  36. 36.
    Li Y, Wang FH, Knox RB (1989) Ultrastructural analysis of the flagellar apparatus in sperm cells of Ginkgo biloba. Protoplasma 149: 57–63CrossRefGoogle Scholar
  37. 37.
    Hori T, Ridge R, Michikawa M, Miyamura S (1988) Ultrastructure of the sperm of Ginkgo biloba (in Japanese). Proc of 53rd Ann Meet Bot Soc Jpn, 13–15 October, Okayama, p 213Google Scholar
  38. 38.
    Hori T, Miyamura S (1996) Further studies on the gametes and fertilization of Ginkgo biloba and Cycas revoluta. Abs of Cent Comme Sym Discovering Ginkgo Sperm, “Biology of Ginkgo biloba.” 8 Sep 1996, University of Tokyo, Tokyo, p 13Google Scholar
  39. 39.
    Hirase S (1895) Études sur le Ginkgo biloba. (Note préliminaire). Bot Mag Tokyo 9: 240–239Google Scholar
  40. 40.
    Hirase S (1918) Nouvelles recherches sur la fécondation et l’embryogénie du Ginkgo biloba. Bot Mag Tokyo 32: 139–144Google Scholar
  41. 41.
    Hirase S (1918) Further studies on the fertilization and embryogeny in Ginkgo biloba (in Japanese). Bot Mag Tokyo 32: 83–108Google Scholar
  42. 42.
    Ikeno S (1901) Contribution a l’étude de la fécondation chez le Ginkgo biloba. Ann Sc Nat Bot ser. 8 13: 305–316Google Scholar
  43. 43.
    Shimamura T (1928) On the formation of proembryo of Ginkgo biloba L (in Japanese). Bot Mag Tokyo 42:71–76, 77–82Google Scholar
  44. 44.
    Shimamura T (1931) A note on the mitotic division in the proembryo of Ginkgo, with special reference to a chromatin-elimination (in Japanese with English resume). Bot Mag Tokyo 45: 525–530Google Scholar
  45. 45.
    Shimamura T (1935) Zur Cytologie des Befruchtungsvorganges bei Cycas und Ginkgo unter Benutzung der Feulgenschen Nuklearreaktion. Cytologia 6: 465–473CrossRefGoogle Scholar
  46. 46.
    Favre-Duchartre M (1958) Ginkgo, an oviparous plant. Plantmorphology 8: 377–390Google Scholar
  47. 47.
    De Sloover-Colinet A (1962) Chambre pollinique et gamétophyte mâle chez Ginkgo biloba. Cellule 64: 129–145Google Scholar
  48. 48.
    Camefort H (1965) L’organisation du protoplasme dans le gamète femelle, ou oosphère, du Ginkgo biloba L. J Microscopie 4: 531–546Google Scholar
  49. 49.
    Soma S, Kaneko F, Kasai H, Yokomizo C (1986) Fertilization in Ginkgo biloba (in Japanese). Ann Rep Fac Edu Bunkyo Univ No. 20: 67–74Google Scholar
  50. 50.
    Sterling C (1963) Structure of the male gametophyte in gymnosperms. Biol Rev 38: 167–203PubMedCrossRefGoogle Scholar
  51. 51.
    Jeffrey EC (1914) Spore conditions in hybrids and the mutation hypothesis of de Vries. Bot Gaz 58: 322–336CrossRefGoogle Scholar
  52. 52.
    Chamberlain CJ (1898) The homology of the blepharoplast. Bot Gaz 26: 431–435CrossRefGoogle Scholar
  53. 53.
    Webber H (1897) Peculiar structures occurring in the pollen tube of Zamia. Bot Gaz 23: 453–459CrossRefGoogle Scholar
  54. 54.
    Mizukami I, Gall J (1966) Centriole replication II. Sperm formation in the fern, Marsilea, and the cycad, Zamia. J Cell Biol 29: 97–111Google Scholar
  55. 55.
    Chamberlain CJ (1909) Spermatogenesis in Dioon edula. Bot Gaz 47: 215–236CrossRefGoogle Scholar
  56. 56.
    Kuwada Y, Maeda T (1929) On the structure of the cytoplasm around the blepharoplast in Cycas revoluta. Mem Coll Sci Kyoto Imp Univ 4: 165–174Google Scholar
  57. 57.
    Herzfeld S (1928) Über die Kernteilungen in Proembryo von Ginkgo biloba. Jahrb Wiss Bot 66: 264–294Google Scholar
  58. 58.
    Chamberlain CJ (1912) Morphology of Ceratozamia. Bot Gaz 53: 1–19CrossRefGoogle Scholar
  59. 59.
    Wolniak SM (1976) Organelle distribution and apportionment during meiosis in the microsporocyte of Ginkgo biloba L. Amer J Bot 63: 251–258CrossRefGoogle Scholar
  60. 60.
    Hori T, Miyamura (1991) Analysis of the releasing process of the sperms in Cycas revoluta by high-speed video (in Japanese). Proc of 56th Ann Meet Bot Soc Jpn, 13–15 September, Tokyo, p 125Google Scholar
  61. 61.
    Foster AS, Gifford EM (1974) Comparative morphology of vascular plants, 2nd edn. WH Freeman, San Francisco, 751 ppGoogle Scholar
  62. 62.
    Ferguson MC (1901) The development of the egg and fertilization in Pinus Strobus. Ann Bot 15: 435–479Google Scholar
  63. 63.
    Hori T, Miyamura S (1990) Analysis of the fertilization process of Cycas revoluta by high-speed video (in Japanese). Proc of 55th Ann Meet Bot Soc Jpn, 2–4 October, Shizuoka, p 137Google Scholar
  64. 64.
    Schnarf K (1933) Embyologie der Gymnospermen. In: Hand Pflanzenana 10/2, BerlinGoogle Scholar
  65. 65.
    Hori T (1989) Ultrastructural reinvestigation on fertilization of the gymnosperm, Cycas revoluta (in Japanese). Proc of 54th Ann Meet Bot Soc Jpn, 27–29 September, Sendai, p 174Google Scholar
  66. 66.
    Chamberlain CJ (1916) Stangeria paradoxa. Bot Gaz 61: 353–372CrossRefGoogle Scholar
  67. 67.
    Lawson A (1926) A contribution to the life history of Bowenia. Trans Roy Soc Edin 54: 357–393Google Scholar
  68. 68.
    Swamy BGL (1948) Contributions to the life history of a cycas from Mysore (India). Amer J Bot 35: 77–88CrossRefGoogle Scholar
  69. 69.
    de Silva BLT, Tambiah MS (1952) A contribution to the life history of Cycas rumphii Miq. Ceylon J Sei (A) 12: 223–244Google Scholar
  70. 70.
    Gifford EM, Foster AS (1989) Morphology and evolution of vascular plants, 3rd edn. WH Freeman, New York, 626 ppGoogle Scholar
  71. 71.
    Hori T, Miyamura S (1993) Cytological and video analysis of fertilization in Cycas revoluta. Abs of XV Int Bot Con, 28 August-3 September, Yokohama, p 96Google Scholar
  72. 72.
    Ikeno S (1898) Untersuchungen über die Entwickelung der Geschlechtsorgane und den Vorgang der Befruchtung bei Cycas revoluta. Jahrb Wiss Bot 32: 557–602Google Scholar
  73. 73.
    Webber HJ (1901) Spermatogenesis and fecundation of Zamia. US Dept Agricul Ber Plant Ind Bull Washington No. 2: 1–92Google Scholar
  74. 74.
    Brough P, Taylor MH (1940) An investigation of the life cycle of Macrozamia spiralis Miq. Proc Linn Soc New South Wales 65: 494–524Google Scholar
  75. 75.
    Blackman VH (1898) On the cytological features of fertilization and related phenomena in Pinus silvestris L. Phil Trans Roy Soc London Ser B 190: 395–426CrossRefGoogle Scholar
  76. 76.
    Jäger L (1899) Beiträge zur Kenntnis der Endospermbildung und zur Embryologie von Taxus baccata L. Flora 86: 241–288Google Scholar
  77. 77.
    Arnoldi W (1900) Beiträge zur morphologie der Gymnospermen: III. Embryogenie von Cephalotaxus Fortunei. Flora 87: 46–63Google Scholar
  78. 78.
    Miyake K (1903) Contribution to the fertilization and embryogeny of Abies balsamea. Beih Bot Centr 14: 134–144Google Scholar
  79. 79.
    Hirase S (1918) On the fertilization of Pinus Thumbergii Pari. Bot Mag Tokyo 32: 343–356Google Scholar
  80. 80.
    Norstog K, Overstreet R (1965) Some observations on the gametophytes of Zamia integrifolia. Phytomorphology 15: 46–49Google Scholar
  81. 81.
    Norstog K (1975) The motility of cycad spermatozoids in relation to structure and function. In: Duckett JG, Racey PA (eds) The biology of the male gamete. Academic, London, pp 135–142Google Scholar
  82. 82.
    Bryan GS, Evans RI (1956) Chromatin behavior in the development and maturation of the egg nucleus of Zamia umbrosa. Amer J Bot 43: 640–646CrossRefGoogle Scholar
  83. 83.
    Bryan GS, Evans RI (1957) Types of development from the central nucleus of Zamia umbrosa. Amer J Bot 44: 404–415CrossRefGoogle Scholar
  84. 84.
    Baird AM (1939) A contribution to the life history of Macrozamia reidlei. J Roy Soc W Aust 25: 153–175Google Scholar
  85. 85.
    Lang WH (1900) Studies in the development and morphology of cycadean sporangia: II. The ovule of Stangeria paradoxa. Ann Bot 14: 281–306Google Scholar
  86. 86.
    Barner H, Christiansen H (1960) The formation of pollen, the pollination mechanism, and the determination of the most favourable time for controlled pollinations in Larix. Silv Gen 9: 1–11Google Scholar
  87. 87.
    Camefort H (1967) Observations sur les mitochondries et les plastes de la cellule centrale et de l’oosphère du Larix decidua Mill (Larix europea D.C.). C R Acad Se Paris 265: 1293–1294Google Scholar
  88. 88.
    Camefort H (1967) Fécondation et formation d’un néocytoplasme chez le Larix decidua Mill. (Larix europea D.C.). C R Acad Se Paris 265: 1784–1787Google Scholar
  89. 89.
    Owens JN, Molder M (1979) Sexual reproduction of Larix occidentalis. Can J Bot 57: 2673–2690CrossRefGoogle Scholar
  90. 90.
    Allen GS (1943) The embryogeny of Pseudotsuga taxifolia (Lamb.) Britt. Amer J Bot 30: 655–661CrossRefGoogle Scholar
  91. 91.
    Allen GS (1946) Embryogeny and development of the apical meristem of Pseudotsuga. I. Fertilization and early embryogeny. Amer J Bot 33: 666–677CrossRefGoogle Scholar
  92. 92.
    Owens JN, Morris SJ (1990) Cytological basis for cytoplasmic inheritance in Pseudotsuga menziesii. I. Pollen tube and archegonial development. Amer J Bot 77: 433–445Google Scholar
  93. 93.
    Sugiura Y (1943) Embryological observations on Keteleeria davidiana Beissner var. formosana Hayata. Sci Rep Tohoku Imp Univ 17: 215–222Google Scholar
  94. 94.
    Wang FH (1948) Life history of Keteleeria. I. Strobili, development of the gametophytes and fertilization in Keteleeria evelyniana. Amer J Bot 35: 21–27CrossRefGoogle Scholar
  95. 95.
    Haupt AW (1941) Oogenesis and fertilization in Pinus lambertiana and P. monophylla. Bot Gaz 102: 482–498CrossRefGoogle Scholar
  96. 96.
    Shimamura T (1956) Cytochemical studies on the fertilization and proembryo of Pinus Thunbergii (in Japanese). Bot Mag Tokyo 69: 524–529Google Scholar
  97. 97.
    Konar RN, Ramchandani S (1958) The morphology and embryology of Pinus wallichiana Jack. Phytomorphology 8: 328–346Google Scholar
  98. 98.
    McWilliam JR, Mergen F (1958) Cytology of fertilization in Pinus. Bot Gaz 119: 246–249CrossRefGoogle Scholar
  99. 99.
    Konar RN (1962) Some observations on the life history of Pinus geradiana Wall. Phytomorphology 12: 196–201Google Scholar
  100. 100.
    Camefort H (1965) Étude en microscopie électronique de la fécondation et de la première mitose du zygote chez le Pinus laricio Poir. var. austriaca (P. nigra Arn.). C R Acad Se Paris 261: 4479–482Google Scholar
  101. 101.
    Lill BS (1976) Ovule and seed development in Pinus radiata: postmeiotic development, fertilization, and embryogeny. Can J Bot 54: 2141–2154CrossRefGoogle Scholar
  102. 102.
    Hutchinson AH (1915) Fertilization in Abies balsamea. Bot Gaz 60: 457–472CrossRefGoogle Scholar
  103. 103.
    Sugiura Y (1947) The embryogeny of Abies firma Siebold et Zuccarini. Bot Mag Tokyo 60: 58–62Google Scholar
  104. 104.
    Singh H, Owens JM (1981) Sexual reproduction in subalpine fir ( Abies lasiocarpa ). Can J Bot 59: 2650–2666Google Scholar
  105. 105.
    Miyake K, Yasui K (1911) On the gametophyte and embryo of Pseudolarix. Ann Bot 25: 639–647Google Scholar
  106. 106.
    Miyaka K (1903) On the development of the seuxl organs and fertilization in Picea excelsa. Ann Bot 17: 351–372Google Scholar
  107. 107.
    Owens JN, Molder M (1979) Sexual reproduction of white spruce ( Picea glauca ). Can J Bot 57: 152–169Google Scholar
  108. 108.
    Owens JN, Molder M (1980) Sexual reproduction of Sitka spruce ( Picea sitchensis ). Can J Bot 58: 886–901Google Scholar
  109. 109.
    Murrill WA (1900) The development of the archegonium and fertilization in the hemlock spruce (Tsuga canadensis, Carr.). Ann Bot 14: 583–607Google Scholar
  110. 110.
    Stanlake E A, Owens JN (1974) Female gametophyte and embryo development in western hemlock ( Tsuga heterophylla ). Can J Bot 52: 885–893Google Scholar
  111. 111.
    Owens JN, Molder M (1975) Sexual reproduction of mountain hemlock ( Tsuga mertensiana ). Can J Bot 53: 1811–1826Google Scholar
  112. 112.
    Chowdhury CR (1961) The morphology and embryology of Cedrus deodara (Roxb.) Loud. Phytomorphology 11: 283–304Google Scholar

Copyright information

© Springer-Verlag Tokyo 1997

Authors and Affiliations

  • Terumitsu Hori
    • 1
  • Shin-ichi Miyamura
    • 1
  1. 1.Institute of Biological SciencesUniversity of TsukubaTsukuba, Ibaraki 305Japan

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