Development of the Male Gametophyte of Ginkgo biloba: A Window into the Reproductive Biology of Early Seed Plants

  • William E. Friedman
  • Ernest M. Gifford


It has been a century since the discovery of zooidogamous reproduction among seed plants by Hirase [1, 2] and Ikeno [3]. The initial observations of motile sperm in Ginkgo and Cycas represented the culmination of progress, beginning with the discovery of the pollen tube by Amici [4], in the field of plant reproductive biology during the nineteenth century. Discovery of zooidogamy in Ginkgo and cycads in 1896 provided a critical connection, in terms of evolutionary history, between the life cycles of non-seed plants (“cryptogams”) with motile sperm and the life cycles of previously described seed plants (conifers and angiosperms) with pollen tubes and non-motile sperm [5]. Moreover, the presence of motile sperm within the male gametophytes of cycads and Ginkgo confirmed a prediction made almost one half century earlier by the renowned biologist Wilhelm Hofmeister [6] that flagellate sperm might be found among representatives of the seed plants [5].


Pollen Tube Sperm Cell Seed Plant Female Gametophyte Male Gametophyte 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Hirase S (1896a) Spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 10: 171–172Google Scholar
  2. 2.
    Hirase S (1896b) On the spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 10: 325–328Google Scholar
  3. 3.
    Ikeno MS (1896) Spermatozoid of Cycas revoluta (in Japanese). Bot Mag Tokyo 10: 367–368Google Scholar
  4. 4.
    Amici GB (1824) Observations microscopiques sur diverses espèces de plantes. Ann Sei Nat Bot 2:41–70, 211–248Google Scholar
  5. 5.
    Ikeno S, Hirase S (1897) Spermatozoids in gymnosperms. Ann Bot 11: 344–345Google Scholar
  6. 6.
    Hofmeister W (1851) Vergleichende Untersuchungender Keimung, Entfaltung, und Fruchtbildung horerer Kryptogamen und der Samenbildung der Coniferen. Fr Hofmeister, LeipzigGoogle Scholar
  7. 7.
    Hirase S (1894) Notes on the attraction-spheres in the pollen-cells of Ginkgo biloba. Bot Mag Tokyo 8: 359–360Google Scholar
  8. 8.
    Hirase S (1895a) Études sur le Ginkgo biloba. Bot Mag Tokyo 9: 238–239Google Scholar
  9. 9.
    Hirase S (1895b) Études sur la fécondation et l’embryogénie du Ginkgo biloba. J Coll Sei Imp Univ Tokyo 8: 307–322Google Scholar
  10. 10.
    Hirase S (1897) Untersuchungen über das Verhalten des Pollens von Ginkgo biloba. Bot Zbl 49: 33–35Google Scholar
  11. 11.
    Hirase S (1898) Études sur la fécondation et l’embryogénie du Ginkgo biloba. J Coll Sei Imp Univ Tokyo 12: 103–149Google Scholar
  12. 12.
    Hirase S (1918) Nouvelles recherches sur la fécondation et l’embryogénie du Ginkgo biloba. Bot Mag Tokyo 32: 139–143Google Scholar
  13. 13.
    Mann MC (1924) Microsporogenesis of Ginkgo biloba L. with special reference to the distribution of plastids and to cell wall formation. Univ Calif Pub Agric Sei 2: 243–248Google Scholar
  14. 14.
    Wolniak SM (1976) Organelle distribution and apportionment during meiosis in the microsporocyte of Ginkgo biloba L. Amer J Bot 63: 251–258CrossRefGoogle Scholar
  15. 15.
    Strasburger E (1892) Über das Verhalten des Pollen und die Befructungs vor gange bei der Gymnospermen. Histol Beitrage Heft 4: 1–158Google Scholar
  16. 16.
    Lee CL (1955) Fertilization in Ginkgo biloba. Bot Gaz 117: 79–100CrossRefGoogle Scholar
  17. 17.
    Webber HJ (1901) Spermatogenesis and fecundation of Zamia. Bull US Dep Agric 2: 1–100Google Scholar
  18. 18.
    Favre-Duchartre M (1956) Contribution a l’etude de la reproduction chez le Ginkgo biloba. Rev Cytol Biol Veg 17: 1–218Google Scholar
  19. 19.
    DeSloover-Colinet A (1963) Chambre pollinique et gametophyte male chez Ginkgo biloba. Cellule 64: 129–145Google Scholar
  20. 20.
    Friedman WE (1987a) Growth and development of the male gametophyte of Ginkgo biloba within the ovule (in vivo). Amer J Bot 74: 1797–1815CrossRefGoogle Scholar
  21. 21.
    Tulecke WR (1957) The pollen of Ginkgo biloba: in vitro culture and tissue formation. Amer J Bot 44: 602–608CrossRefGoogle Scholar
  22. 22.
    Dexheimer J (1970) Recherches cytophysiologiques sur les grains de pollen. Rev Cytol Biol Veg 33: 169–234Google Scholar
  23. 23.
    Rohr R (1980) Développement in vitro du pollen de Ginkgo biloba. Cytologia 45: 481–495CrossRefGoogle Scholar
  24. 24.
    Friedman WE (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
  25. 25.
    Friedman WE, Gifford EM (1988) Division of the generative cell and late development in the male gametophyte of Ginkgo biloba. Amer J Bot 75: 1434–1442CrossRefGoogle Scholar
  26. 26.
    Herzfeld S (1927) Beitrage zur Kenntnis von Ginkgo. Jb F Wiss Bot 66: 814–862Google Scholar
  27. 27.
    Fujii K (1898) Has the spermatozoid of Ginkgo a tail or none? (In Japanese) Bot Mag Tokyo 12: 287–290Google Scholar
  28. 28.
    Fujii K (1899a) Observation on the morphology of the pollen tube and the spermatozoid of Ginkgo (in Japanese). Bot Mag Tokyo 13: 28–30Google Scholar
  29. 29.
    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
  30. 30.
    Fujii K (1899c) On the morphology of the spermatozoid of Ginkgo biloba (in Japanese). Bot Mag Tokyo 13: 260 - 266Google Scholar
  31. 31.
    Fujii K (1900) On bicephalous spermatozoid of Ginkgo (in Japanese). Bot Mag Tokyo 14: 16 - 17Google Scholar
  32. 32.
    Ikeno S (1899a) On the spermatozoid and pollen tube of Ginkgo biloba and Cycas revoluta (in Japanese). Bot Mag Tokyo 13: 31 - 34Google Scholar
  33. 33.
    Ikeno S (1899b) Opinion of various authors on the centrosome in the pollen tube of Cycadaceae and Ginkgo (in Japanese). Bot Mag Tokyo 13: 74 - 76Google Scholar
  34. 34.
    Ikeno S (1901) Contribution a l’étude de la fécondation chez le Ginkgo biloba. Ann Sei Nat Bot 13: 305–318Google Scholar
  35. 35.
    Miyake K (1902) The spermatozoids of Ginkgo. J Appl Lab Meth 5: 1773–1780Google Scholar
  36. 36.
    Webber HJ (1897) Notes on the fecundation of Zamia and the pollen tube apparatus of Ginkgo. Bot Gaz 24: 225–235CrossRefGoogle Scholar
  37. 37.
    Shimamura T (1937) On the spermatozoid of Ginkgo biloba. Cytologia (Fujii Jubilaei): 416–423Google Scholar
  38. 38.
    Gifford EM, Lin J (1974) Ultrastructure des cellules spermatogenes de Ginkgo biloba, et particulièrement du blepharoplaste (mastigosome). C R Acad Sei (Paris) 278: 2513–2515Google Scholar
  39. 39.
    Gifford EM, Lin J (1975) Light microscope and ultrastructural studies of the male gametophyte in Ginkgo biloba: the spermatogenous cell. Amer J Bot 62: 974–981CrossRefGoogle Scholar
  40. 40.
    Gifford EM, Larson S (1980) Developmental features of the spermatogenous cell in Ginkgo biloba. Amer J Bot 67: 119–124CrossRefGoogle Scholar
  41. 41.
    Li Y, Wang FH, Knox RB (1989) Ultrastructural analysis of the flagellar apparatus in sperm cells of Ginkgo biloba. Protoplasma 149: 57–63CrossRefGoogle Scholar
  42. 42.
    Friedman WE (1993) The evolutionary history of the seed plant male gametophyte. Trends Ecol Evol 8: 15–20PubMedCrossRefGoogle Scholar
  43. 43.
    Sterling C (1963) Structure of the male gametophyte in gymnosperms. Biol Rev 38: 167–203PubMedCrossRefGoogle Scholar
  44. 44.
    Chamberlain CJ (1909) Spermatogenesis in Dioon edule. Bot Gaz 47: 215–236CrossRefGoogle Scholar
  45. 45.
    Coulter JM, Chamberlain CJ (1917) Morphology of gymnosperms. Second edition. University of Chicago Press, ChicagoGoogle Scholar
  46. 46.
    Swamy BGL (1948) Contributions to the life history of a Cycas from Mysore (India). Amer J Bot 35: 77–88CrossRefGoogle Scholar
  47. 47.
    Gifford EM, Foster AS (1987) Morphology and evolution of vascular plants. Third edition. WH Freeman, New YorkGoogle Scholar
  48. 48.
    Chaloner WG (1970) The evolution of miospore polarity. Geosci Man 1: 47–56CrossRefGoogle Scholar
  49. 49.
    Taylor TN, Millay MA (1979) Pollination biology and reproduction in early seed plants. Rev Palaeobot Palynol 27: 329–355CrossRefGoogle Scholar
  50. 50.
    Doyle JA (1987) Pollen evolution in seed plants: A cladistic perspective. J Palynol 23 24: 7–18Google Scholar
  51. 51.
    Haig D, Westoby M (1989) Selective forces in the emergence of the seed habit. J Linn Soc 39: 215–238CrossRefGoogle Scholar
  52. 52.
    Crane PR (1990) The phylogenetic context of microsporogenesis. In: Microspores: evolution and ontogeny. Acad Pr pp 11–41Google Scholar
  53. 53.
    Millay MA, Taylor TN (1976) Evolutionary trends in fossil gymnosperm pollen. Rev Palaeobot Palynol 21: 65–91CrossRefGoogle Scholar
  54. 54.
    Kerp JHF, Poort RJ, Swinkels HAJM, Verwer R (1990) Aspects of Permian paleobotany and palynology. IX. Conifer-dominated Rotliegend floras from the Saar-Nahe Basin (Late Carboniferous-Early Permian; SW-Germany) with special reference to the reproductive biology of early conifers. Rev Palaeobot Palynol 62: 205–248Google Scholar
  55. 55.
    Stewart, WN (1951) A new Pachytesta from the Berryville locality of Southeastern Illinois. Amer Midland Nat 46: 717–742CrossRefGoogle Scholar
  56. 56.
    Taylor TN, Daghlian CP (1980) The morphology and ultrastructure of Gothania ( Cordaitales) pollen. Rev Palaeobot Palynol 29: 1–14Google Scholar
  57. 57.
    Steeves TA (1983) The evolution and biological significance of seeds. Can J Bot 61: 3550–3560CrossRefGoogle Scholar
  58. 58.
    Chaloner WG (1976) The evolution of adaptive features in fossil exines. In: The evolutionary significance of the exine. Academic, London, pp 1–14Google Scholar

Copyright information

© Springer-Verlag Tokyo 1997

Authors and Affiliations

  • William E. Friedman
    • 1
  • Ernest M. Gifford
    • 2
  1. 1.Department of EPO BiologyUniversity of ColoradoBoulderUSA
  2. 2.Section of Plant BiologyUniversity of CaliforniaDavisUSA

Personalised recommendations